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

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Abstract and Figures

Four new genera and six new species of fossil seed (Buarcospermum tetragonium, Lignierispermum maroneae, Lobospermum glabrum, L. rugosum, L. stampanonii, Rugonella trigonospermum) are described from five Early Cretaceous mesofossil floras from Portugal and eastern North America. The four genera are distinguished by differences in size, shape, and details of seed anatomy, but all are unusual in having an outer seed envelope with a distinctive anatomical structure that surrounds the nucellus and the integument. The integument is extended apically into a long, narrow micropylar tube. The four new genera are part of a diverse, but previously unrecognized, complex of extinct plants that was widespread in Early Cretaceous vegetation and that coexisted in similar habitats with early angiosperms. The distinctive structure of these seeds, and the strong similarities to other fossil seeds (Ephedra, Ephedripites, Erdtmanispermum, Raunsgaardispermum, and some Bennettitales) already known from the Early Cretaceous, suggests that this newly recognized complex of extinct plants, together with Bennettitales, Erdtmanithecales, and Gnetales (the BEG group), is phylogenetically closely related.
, 23. Buarcospermum tetragonium from the Early Cretaceous (late Aptian or early Albian) Buarcos locality, Portugal, holotype (S101535 sample Buarcos 210). Figs. 20 – 22. Buarcospermum tetragonium from Early Cretaceous (late Barremian-Aptian) Catefi ca locality, Portugal (S156369, sample Catefi ca 382); SRXTM images showing reconstructed slice data of internal structure. Scale bars: Figs. 15, 23 (vertical scale at Fig. 15 ) = 0.5 mm; Figs. 16 – 19 (vertical scale at Fig. 19 ) = 0.5 mm. Figs. 20 – 22 (vertical scale at Fig. 20) = 0.5 mm. Heavy gold coating seen as outer, light covering in Figs. 15 – 19, 23. 15. Longitudinal section (LS) showing micropylar tube, micropylar canal, closure tissue, integument, and nucellus: note micropylar tube fi lled with closure tissue and strongly adpressed to outer envelope. 16. Transverse section (TS) through tip of seed showing central micropylar canal formed by the thin micropylar tube and surrounded by sclerenchyma of the envelope: at the apex, the micropylar tube consists of one cell layer (inner epidermis). 17. TS below Fig. 16 showing the micropylar canal formed by the micropylar tube surrounded by sclerenchyma of the envelope: micropylar tube consists of two cell layers (inner and outer epidermis). 18. TS below Fig. 17 (around the middle of the micropylar tube above the four valves of the seed envelope) showing micropylar canal occluded by closure tissue: closure tissue comprised of radially elongate cells of inner epidermis of micropylar tube with several additional outer cell layers (continuous with outer epidermis of Fig. 17 , see also Fig. 15 ). 19. TS near base of the micropylar tube below Fig. 18 showing tips of the four valves of the seed envelope and closed micropylar canal. 20. LS of micropylar region showing seed envelope surrounding micropylar tube with distinct inner epidermis and open micropylar canal that extends for most of its length (see Figs. 21, 22). 21. TS showing narrow, central micropylar canal formed by the thin micropylar tube surrounded by sclerenchyma layer of the seed envelope: micropylar tube consisting of one cell layer (inner epidermis). 22. TS below Fig. 21 showing narrow, central micropylar canal surrounded by the micropylar tube consisting of two cell layers (inner and outer epidermis). 23. TS showing transition zone between inner and outer sclerenchyma layers of seed envelope.
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252
American Journal of Botany 96(1): 252–283. 2009.
For more than a century, the origin and rise to dominance of
angiosperms, the most diverse group of plants on Earth often
referred to as Darwin s abominable mystery (See Friedman,
2009, pp. 5 21) has been a topic of great botanical interest,
and over the last 30 years concerted efforts at several frontiers
of plant science, have begun to yield an increasingly con-
vincing and coherent picture of early angiosperm diversifi ca-
tion. In systematics, the application of new molecular and
computational tools, combined with advances in phylogenetic
theory, have clarifi ed phylogenetic patterns among living an-
giosperms and have established well-corroborated hypotheses
of branching patterns at the base of the angiosperm phyloge-
netic tree (e.g., Chase et al., 1993 ; Qiu et al., 1999 ; Soltis et al.,
2002 ; Qiu, 2005 ). In comparative morphology renewed and
more focused investigations have revealed unexpected diver-
sity among presumed primitive angiosperms and have nar-
rowed some of the gaps in structure and biology that separate
angiosperms from related seed plants (e.g., Endress, 2001 ;
Friedman, 2006 ). And in palaeobotany, remarkable discoveries
of well-preserved angiosperm reproductive structures have pro-
vided direct insights into the changing systematic relationships
and biology of angiosperms as they increased in diversity and
ecological prominence through the fi rst 70 million years of their
evolutionary history (e.g., Friis et al., 2006 ).
Despite this progress, there are many aspects of angiosperm
evolution that still remain to be understood, but the most sig-
nifi cant remaining problem is to develop a well-corroborated
hypothesis of the phylogenetic position of angiosperms in rela-
tion to other groups of seed plants. Until a consensus emerges
on this issue that can account for both molecular and morpho-
logical data, our understanding of early angiosperm evolution
will remain incomplete.
This key question and others relating to the origin of angio-
sperms are unlikely to be resolved satisfactorily by studies of
living plants alone because the four living groups of nonangio-
sperm seed plants provide only poor representation of the diver-
sity of seed plants that existed in the past. On the basis of the
paleontological record, one or several extinct groups of seed
plants seem very likely to ultimately be shown to be more
closely related to angiosperms than to conifers, cycads, Ginkgo
L., or Gnetales ( Crane et al., 2004 ). Identifi cation of these ex-
tinct groups is crucial to an improved understanding of how the
unique reproductive structures of angiosperms should be prop-
erly compared to those other seed plants. And in turn, this is
vital to understanding how angiosperm stamens, ovules, and
carpels may have evolved. The current situation therefore pro-
vides new opportunities for palaeobotanical research to contrib-
ute to the resolution of an important evolutionary problem at a
time when new techniques and newly discovered fossil material
are also opening up new areas for research.
In this paper, we describe four new genera of fossil seeds
from the Early Cretaceous of Europe and eastern North
America that expand the diversity of seed plants known from
the critical interval when angiosperms were undergoing their
initial diversifi cation. These seeds are of paleoecological in-
terest because they co-occur with fossils of early angiosperms.
1 Manuscript received 29 March 2008; revision accepted 13 October 2008.
The authors thank J.-P. and M. Rioult for valuable information and help
in retrieving the original specimen of Cycadeoidea morierei . They also
thank P. von Knorring for preparing the line drawings, M. von Balthazar
for preparing some of the Puddledock specimens, and M. Stampanoni, F.
Marone, S. Bengtson, and T. Huldtgren for help with SRXTM and PCXTM
analyses at the Swiss Light Source, Paul Scherrer Institut, Villigen,
Switzerland. This research project has been supported by the European
Commission under FP6: Strengthening the European Research Area,
Research Infrastructures: project no. 20070197 (to P. C. J. Donoghue, S.
Bengtson, and E. M. Friis), by the Swedish Natural Science Research
Council (E. M. Friis), the Carlsberg Foundation (K. R. Pedersen), and the
U.S. National Science Foundation (P. R. Crane).
5 Author for correspondence (e-mail: else.marie.friis@nrm.se)
doi:10.3732/ajb.0800113
E ARLY CRETACEOUS MESOFOSSILS FROM
P ORTUGAL AND EASTERN NORTH AMERICA RELATED TO
THE BENNETTITALES-ERDTMANITHECALES-GNETALES GROUP 1
Else Marie Friis, 2,5
Kaj Raunsgaard Pedersen,
3
and Peter R. Crane
4
2 Department of Palaeobotany, Swedish Museum of Natural History, SE-104 05 Stockholm, Sweden;
3 Department of Geology,
University of Aarhus, DK-8000 Å rhus C, Denmark; and
4 Department of the Geophysical Sciences, University of Chicago,
Chicago, Illinois 60637 USA
Four new genera and six new species of fossil seed ( Buarcospermum tetragonium , Lignierispermum maroneae , Lobospermum
glabrum, L. rugosum, L. stampanonii , Rugonella trigonospermum ) are described from fi ve Early Cretaceous mesofossil fl oras
from Portugal and eastern North America. The four genera are distinguished by differences in size, shape, and details of seed
anatomy, but all are unusual in having an outer seed envelope with a distinctive anatomical structure that surrounds the nucellus
and the integument. The integument is extended apically into a long, narrow micropylar tube. The four new genera are part of a
diverse, but previously unrecognized, complex of extinct plants that was widespread in Early Cretaceous vegetation and that co-
existed in similar habitats with early angiosperms. The distinctive structure of these seeds, and the strong similarities to other fossil
seeds ( Ephedra , Ephedripites , Erdtmanispermum , Raunsgaardispermum , and some Bennettitales) already known from the Early
Cretaceous, suggests that this newly recognized complex of extinct plants, together with Bennettitales, Erdtmanithecales, and
Gnetales (the BEG group), is phylogenetically closely related.
Key words: anthophytes; BEG group; ephedroids; extinct seed plants; fossil seeds; PCXTM; seed plant phylogeny; SRXTM;
synchrotron-radiation X-ray tomographic microscopy.
253
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
correspond to the lower couches d Almargem that in the Torres Vedras area
range from late Barremian to late Aptian in age ( Rey, 1993 ; Rey et al., 2006 ).
Fossil plants were extracted from samples 49, 154, 242 and 382 collected in
1989, 1992, 1997, and 2001, respectively (K.R.P., E.M.F. with P.R.C. in 1989).
The mesofl ora comprises several different kinds of gymnosperm seeds includ-
ing ephedroid seeds and the seeds described here, as well as twigs of cheirole-
pidiaceous conifers. The Catefi ca locality has also yielded many angiosperm
owers, fruits, seeds, and stamens with pollen in situ including a variety of
chloranthaceous reproductive structures that are similar to material from the
Torres Vedras locality ( Friis et al., 1994b , 1999 , 2000b , 2006 ).
The Torres Vedras locality is a large open-cast clay pit in the northeastern
outskirts of Torres Vedras, about 1 km NE of Forte de Forca on the road toward
Sarge, Portugal (39 ° 06 13 ” N, 9 ° 14 47 ” W) (Carta Geol ó gica de Portugal Torres
Vedras 30C, Zbyszewski et al. [1955]). The fossils were recovered from sample
45, collected in 1989 (K.R.P., E.M.F., P.R.C.) from a sandy lignitic horizon just
below a prominent ferruginous crust. The locality is no longer accessible and
has been overtaken by urban development. Sediments in this area belong to the
Lugar d Almen Formation, the Fonte Granda Formation, and the Almargem
Formation. Samples from the lignitic horizon belong to the lower part of the
Almargem Formation, which is regarded in this area as late Barremian-early
Aptian in age ( Rey, 1993 ; see also Friis et al., 2004 ). Mayoa portugallica Friis,
Pedersen et Crane, based on a clump of characteristic pollen ( Friis et al., 2004 ),
was recovered from sample 44 at the Torres Vedras locality and has been as-
signed to Araceae. The fl ora also includes several staminate and pistillate struc-
tures related to Hedyosmum (Chloranthaceae) ( Friis et al., 1994b ).
The Puddledock locality is located south of Richmond, Virginia, USA, east
of the Appomattox River, in Prince George County (37 ° 15 45 N; 77 ° 22 25 W).
A series of mesofossil assemblages have been extracted from samples collected
from the Potomac Group in 1988 (P.R.C., E.M.F., K.R.P. with A.N. Drinnan)
at the Tarmac Lone Star Industries Puddledock sand and gravel pit. Samples
082 and 083 were collected from the uppermost part of an organic rich clay
layer exposed in the northern wall of the Puddledock pit. Further quarrying has
now removed this exposure. Palynological analyses (Christopher in Dischinger,
1987 ) indicate that the Potomac Group sediments at this locality are of late
Early Cretaceous age and can be assigned to the basal part of subzone IIB in the
palynological zonation established by Brenner (1963) and others ( Doyle, 1969 ;
Doyle and Hickey, 1976 ; Doyle and Robbins, 1977 ; Hickey and Doyle, 1977 ).
Subzone IIB is of Middle Albian age but may extend down into the Early Al-
bian ( Doyle, 1992 ). The diverse mesofossil assemblages at the Puddledock lo-
cality include a variety of angiosperm reproductive structures (see Friis et al.,
1994a , 1995 ; von Balthazar et al., 2007 ), as well as remains of conifers ( Srini-
vasan, 1992 , 1995 ) and other seed plants. Among the angiosperms that have
been formally described from the Puddledock locality are angiosperm fl owers
and fruits of Virginianthus calycanthoides Friis, Eklund, Pedersen et Crane
(1994a) , Appomattoxia ancistrophora Friis, Pedersen et Crane, Anacostia vir-
giniensis Friis, Pedersen et Crane (1995) , Potomacanthus lobatus von Balt-
hazar, Pedersen, Crane et Friis (2007) and Carpestella lacunata von Balthazar,
Pedersen, Crane et Friis (2008) . Other seed plants described from the Puddle-
dock locality comprise conifer shoots of Glenrosa virginiensis V. Srinivasan,
Glenrosa hopewellensis V. Srinivasan (1992) , Athrotaxis cf. ungeri (Halle) Flo-
rin, Pseudofrenelopsis nathorstiana V. Srinivasan, Watsoniocladus fl orinii V.
Srinivasan, Watsoniocladus virginiensis V. Srinivasan, and Watsoniocladus sp.
( Srinivasan, 1995 ).
Sediment samples from all fi ve localities were suffi ciently soft to break
down in water. Plant fossils were extracted by wet sieving. Adhering mineral
matrix was removed with 40% HF followed by treatment in 10% HCl and thor-
ough rinsing in water. Fossils were then air dried and sorted using refl ected
light microscopy. Measurements were made by stereomicroscope, using SEM
or from tomographic images. For attenuation-based synchrotron-radiation X-
ray tomographic microscopy (SRXTM) and phase-contrast X-ray tomographic
microscopy (PCXTM) specimens were mounted on small brass stubs without
further treatment. In a few cases, specimens were remounted after they had
been studied in SEM.
SRXTM and PCXTM was performed at the TOMCAT beamline of the
Swiss Light Source of the Paul Scherrer Institut, Switzerland, using the tech-
nique described by Donoghue et al. (2006) and Friis et al. (2007) . One or more
specimens for each of the new species described here were studied using micro-
tomography. For comparison, we also used these same methods for several re-
lated mesofossils and mineralized material. Smaller, coalifi ed seeds were
imaged using a 10 × objective and PCXTM at 20 keV or SRXTM at 10 keV.
Larger, coalifi ed seeds were imaged using a 4 × objective and SRXTM at 10
keV. The micropylar area of Buarcospermum tetragonium and Lignierispermum
maroneae was imaged using a 20 × object and SRXTM at 10 keV to obtain
However, they also exhibit a common set of unusual structural
features that unite them as part of a previously unrecognized
complex of extinct plants that was diverse and widespread in
the Early Cretaceous. In addition, strong similarities between
seeds of this complex and previously described seeds of Ben-
nettitales, Erdtmanithecales, and fossil and living Gnetales
(BEG) provide evidence of a probable close relationship ( Friis
et al., 2007 ). If this BEG group is supported by additional ob-
servations and analyses it may have important implications for
understanding the origin of angiosperms because previous phy-
logenetic analyses (e.g., Crane, 1985 ; Hilton and Bateman,
2006 ) suggest that angiosperms may be closely related to Gne-
tales and Bennettitales. These ideas need to be tested by addi-
tional analyses and observations as further information
accumulates on these different groups of extinct and living seed
plants.
MATERIALS AND METHODS
The fossil seeds formally described here were recovered from Early Creta-
ceous mesofossil fl oras at four localities in Portugal (Buarcos, Famalic ã o, Cate-
ca, Torres Vedras) and one in eastern North America (Puddledock). The
Buarcos locality is located northwest of Figueira da Foz (Beira Litoral region),
40 ° 09 54 ˝ N, 8 ° 52 11 ˝ W in the town of Buarcos, Portugal (Carta Geol ó gica de
Portugal 19C Figueira da Foz, Rocha et al. [1981]). Samples were collected
from a partly overgrown road cut in 1992, 1994, 1995, 1997, 1999, 2000, and
2001 (by K.R.P., E.M.F.). The fossils described here were extracted from sam-
ples 157, 209, 210, and 211. The plant-bearing sequence from Buarcos is in-
cluded in the Calvaria Member of the Figueira da Foz Formation, the lowermost
member of the formation and is thought to be of late Aptian to early Albian
( Dinis, 2001 ) or early Albian ( Heimhofer et al., 2005 ) age. A small palynofl ora
has been reported from this locality by Pais and Reyre (1981) . Rich mesofossil
assemblages from the Buarcos locality include many reproductive structures
related to early-branching lineages of extant angiosperms ( Friis et al., 1999 ,
2000b ). Cheirolepidiaceous conifers and ephedroid seeds are also common.
Taxa already described from the Buarcos locality include Anacostia lusitanica
Friis, Crane et Pedersen (1997) , Pennicarpus tenuis Friis, Pedersen et Crane
(2000a) , Ephedra portugallica Rydin, Pedersen, Crane et Friis and Ephed-
rispermum lusitanicum Rydin, Pedersen, Crane et Friis (2006a) . Many other
plant fossils of diverse relationships still remain to be formally described.
The Famalic ã o locality is located at a large clay pit on the eastern outskirts
of the small village of Famalic ã o, about 5 km SSE of Leiria, Portugal
(39 ° 42 16 N, 8 ° 46 12 W) (Carta Geol ó gica de Portugal 23-C Leiria, Teixeira
et al. [1968]). The fossils were recovered from sample 25, collected in 1989 (by
K.R.P., E.M.F., P.R.C.) from a layer of dark organic rich clay, more than 1 m
thick. This layer was exposed in a small temporary excavation deep below the
bottom of the pit and was not accessible on subsequent visits to the locality. On
the basis of lithological/stratigraphical studies of the Lower Cretaceous se-
quence in Portugal, Dinis (2001) divided the sedimentary sequence in the Fa-
malic ã o region into a lower Calvaria Member and an upper Famalic ã o Member
of the Figueira da Foz Formation. The Calvaria Member is described as con-
glomeratic and sandy. It is regarded as of late Aptian to early Albian age. The
plant bearing clay, excavated from beneath the fl oor of the Famalic ã o pit, lay
below the Calvaria Member and must be older. We consider it to be of probable
late Aptian age. The rich mesofossil assemblage from Famalic ã o includes more
than hundred different kind of angiosperm fl owers, fruits, and seeds ( Friis et al.,
1999, 2000b ; Eriksson et al., 2000 ) as well as diverse other seed plants. Two
species of angiosperm, Anacostia lusitanica Friis, Crane et Pedersen and Ana-
costia sp., have been formally described from the Famalic ã o locality ( Friis et
al., 1997 ).
The Catefi ca locality is a road cut exposure along the small road between the
villages of Catefi ca and Mugideira about 4 km SSE of Torres Vedras (39 ° 3 30 N,
9 ° 14 30 W). Samples were collected in 1989 (K.R.P., E.M.F., P.R.C.) and
1992 and 1995 (K.R.P., E.M.F.) in fl uviatile cross-bedded sands with interca-
lated clay beds and darker organic rich horizons. The Lower Cretaceous strata
at the Catefi ca locality are deposited in the western margins of the Runa Basin
(Carta Geol ó gica de Portugal 30-D Alenquer, Zbyszewski and Torre de As-
sun ç ã o [1965]). The strata were studied by Rey (1972) who recognized a lower
and an upper couches d Almargem. The sediments at the Catefi ca locality
254 American Journal of Botany [Vol. 96
Holotype — S101535 from sample Buarcos 210, illustrated
Figs. 1, 2, 4, 9 19, 23 .
Paratypes — S156000, S156004 (sample Buarcos 157),
S156001 (sample Buarcos 209), S156002 (sample Buarcos
211), S156212 S156214 (sample Buarcos 371).
Other specimens examined — S156003 (sample Torres Ve-
dras 45), S156215 S156216 (sample Catefi ca 49), S1-
56225 – S156227 (sample Catefi ca 154), S156369 (sample
Catefi ca 382), PP53211, PP53340 (sample Puddledock 082),
PP53695 53697 (sample Puddledock 083).
Type locality — Buarcos, Northwest of Figueira da Foz, Por-
tugal (40 ° 09 54 ˝ N, 8 ° 52 11 ˝ W).
Stratigraphic position and age of type stratum Calvaria
Member, Figueira da Foz Formation. Early Cretaceous (late
Aptian or early Albian).
Description and comments on the species Buarcospermum
tetragonium is based on isolated seeds from four Early Creta-
ceous localities, three in Portugal (Buarcos, Catefi ca, Torres
Vedras), and one in eastern North America (Puddledock).
The seeds are small, ~1.8 2.2 mm long and 1.4 1.5 mm
broad, radially symmetrical, and broadly ovoid. They taper api-
cally into a pointed micropylar region, about 0.25 mm long and
0.06 mm broad ( Figs. 1 6, 8 9 ). In cross-section the seeds are
four-angled ( Figs. 4 6, 11 13 ). The outer surface of the seeds,
where the epidermis is abraded, is characterized by a four-
parted organization with four elongated and pointed segments
that extend from the base of the seed to the base of the micropy-
lar area and are separated from each other by four distinct lon-
gitudinally extended ribs.
The X-ray microtomography of the holotype (S101535) and
an additional specimen (S156369) shows that the seeds are
composed of a thin integument enclosed by a sclerenchymatous
seed envelope ( Figs. 10 23 ). The integument is extended api-
cally and surrounds a very long and narrow micropylar tube,
~0.6 mm long and 0.012 mm wide ( Figs. 10, 15 ). In the apical
region, the integument consists of a single layer of thin-walled
cells, the inner epidermis, which forms a circular ring around
the open micropylar tube ( Figs. 15, 16 , 20, 21). Further down,
an addition cell layer, the outer epidermis, is present ( Figs. 15,
17 , 20, 22). This layer becomes multicellular with small isodia-
metric cells several layers thick toward the middle and base of
the micropylar tube ( Figs. 15, 18 19 ). In the holotype (S101535),
the micropylar canal is closed in the middle and toward the base
by the cells of the inner epidermis that are expanded radially
toward the center of the micropylar tube ( Figs. 15, 18, 19 ). In
specimen S156369, which perhaps represents a younger devel-
opmental stage, the micropylar canal appears to be open for the
full length of the micropylar tube (Figs. 20 22). In both speci-
mens, the micropylar tube is closely adpressed to the seed enve-
lope in the middle and basal part of the micropylar region ( Figs.
10, 11, 15, 18, 19 ).
The integument is surrounded by a robust envelope that
is open only at the apex ( Figs. 10, 15 19, 24 28 ). Integument
and seed envelope are free from each other except at the
base where the integument is broadly attached ( Fig. 10 ).
The integument encloses the nucellus ( Fig. 10 ). Nucellus ap-
pears to be free from the integument apically but fused to it in
the lower part ( Figs. 10, 13 ), but these inner tissues and the
higher resolution of a selected area. Mineralized material was imaged using a 4 ×
objective and SRXTM at 25 keV. Slice data were analyzed and manipulated
using the program AMIRA (Mercury Computer Systems, Merignac Cedex,
France, http://www.tgs.com/products/amira.asp) for computed tomography.
Specimens for SEM were mounted on aluminum stubs and coated with gold for
60 s and studied using a Hitachi S-4300 fi eld emission scanning electron micro-
scope at 2 kV with the exception of specimen S101535 (Holotype for Buar-
cospermum tetragonium ) that was coated with gold for about 7 min and studied
using a Philips 515 scanning electron microscope at 15 kV. Nail polish was used
for mounting specimens for both X-ray and SEM studies with the exception of
some Cycadeoidea morierei seeds that were mounted with wax. Specimens
studied with SRXTM and PCXTM were studied (gold-coated) with SEM either
before or after microtomography.
All the fossil seeds that we describe in this paper have two layers around the
nucellus. To avoid confusion, we describe these seeds in as neutral terms as pos-
sible. The inner layer we refer to as integument, in conformity with standard
descriptions of seeds of conifers, cycads, Ginkgo, Gnetales, and most fossil seed
plants. The outer layer we refer to as the seed envelope. In some previous
studies (e.g., Crane, 1985; Pedersen et al., 1989a ) this layer has been referred to
as cupule. We avoid this term and its potential implications for homology with
structures in other seed plants.
The fossil material formally described in this paper is housed in the palaeo-
botanical collections of the Swedish Museum of Natural History (S) and the
geological collections of the Field Museum, Chicago (PP). In addition, we in-
clude information about material that we have collected from other localities of
Early Cretaceous age. Also included are illustrations of seeds of Cycadeoidea
morierei (Saporta et Marion) Seward from the Early Cretaceous of Vaches-
Noires of Normandy, France (courtesy of the University of Caen).
SYSTEMATICS
Buarcospermum gen. nov .
Derivation of generic name From the Buarcos locality,
Portugal, where the type species was discovered.
Generic diagnosis — Seeds small, radially symmetrical,
broadly ovoid, micropylar region pointed; four-angled in cross
section. Integument thin, micropylar tube long, narrow. Integu-
ment enclosed by a seed envelope, except for the micropylar
opening, and attached to the envelope only at the base. Nucellus
thin, enclosed by the integument; nucellus free distally, other-
wise fused to the integument. Micropyle open at the apex. Be-
low, micropylar closure distinct, multicellular, formed mainly
from a layer of larger cells that are expanded radially toward the
center of the micropylar tube. Inner surface of seed envelope
smooth, nonpapillate; outer surface smooth. Seed envelope with
an inner and outer sclerenchyma layer. Inner sclerenchyma layer
continuous around the integument and surrounding the micro-
pylar tube; circular in transverse section around micropylar tube,
but four-angled below with four narrow wing-like crests radiat-
ing through the outer sclerenchyma layer to the surface and di-
viding it into four valves. Inner sclerenchyma layer almost
circular in transverse section in the middle of the seed. Cells
long, fi brous arching upwards in a chevron pattern and forming
longitudinal ridges toward the outside. Arches short, formed by
the fi bers. Cells of outer sclerenchyma layer short, irregularly
arranged. Demarcation between inner and outer sclerenchyma
layers irregular, with a transitional zone of open spaces.
Type species — Buarcospermum tetragonium sp. nov.
Buarcospermum tetragonium sp. nov. (Figs. 1 28)
Derivation of specifi c epithet Referring to the four-angled
shaped of the seeds.
Specifi c diagnosis — As for the genus.
255
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Figs. 1 – 9. Buarcospermum tetragonium from the Early Cretaceous (late Aptian or early Albian) Buarcos locality, Portugal; SEM images. Scale bars:
Figs. 1 6 = 1 mm; Fig. 7 = 0.1 mm; Fig. 8 = 0.2 mm; Fig. 9 = 0.5 mm. Figs. 1, 2, 4, 9 . Holotype (S101535, sample Buarcos 210). Figs. 3, 8. Paratype
(S156000, sample Buarcos 157). Figs. 5 7 . Paratype (S156004, sample Buarcos 157). 1, 2. Lateral views of seed showing seed envelope with valves (outer
sclerenchyma layer) and projecting inner fi brous tissue (inner sclerenchyma layer). 3. Lateral view showing epidermis partly preserved. 4 . Apical view
showing four-angled outline and four valves of the seed envelope. 5. Broken seed showing the wing-like crests of the inner fi brous layer and the outer valves
of the seed envelope. 6. Broken seed in apical view showing fi brous crests (inner sclerenchyma layer) and valves (outer sclerenchyma layer). 7. Inner epi-
dermis of seed envelope; note transversely elongate fi ber cells below the epidermis. 8. Apical view showing micropylar tube surrounded by the scleren-
chyma layer of the seed envelope and intact outer epidermis. 9. Apical view showing inner fi ber layer and valves of the seed envelope.
256 American Journal of Botany [Vol. 96
Figs. 10 – 14. Buarcospermum tetragonium from the Early Cretaceous (late Aptian or early Albian) Buarcos locality, Portugal; SRXTM images of
holotype (S101535 sample Buarcos 210) showing reconstructed slice data of internal structure. Figs. 10, 14 . Longitudinal sections. Figs. 11 – 13 . Transverse
sections. Scale bars: Figs. 10 13 (vertical scale at Fig. 10 ) = 1 mm; Fig. 14 (horizontal scale) = 0.5 mm. Heavy gold coating seen as outer, light covering.
10. Longitudinal section showing micropylar tube, micropylar canal, closure tissue, integument with basal attachment, and the various layers of the seed
envelope (inner fi ber layer forming the crests, transitional zone, outer sclerenchyma layer forming the valves). 11. Transverse section around the middle of
micropylar tube showing tips of the four valves of the seed envelope, micropylar tube fi lled by the closure tissue and strongly adpressed to seed envelope:
four wing-like crests of the inner fi brous layer extend almost to the surface of seed envelope. 12. Transverse section in the upper part of seed body showing
seed envelope and integument: micropylar tube solid, fi lled by the closure tissue. 13. Transverse section near the middle of seed body showing seed enve-
lope, integument, nucellus, and internal tissues. 14. Longitudinal (tangential) section through the seed envelope showing arched fi bers of inner scleren-
chyma layer, transitional zone, and outer sclerenchyma layer.
257
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Figs. 15 – 19, 23. Buarcospermum tetragonium from the Early Cretaceous (late Aptian or early Albian) Buarcos locality, Portugal, holotype (S101535
sample Buarcos 210). Figs. 20 22. Buarcospermum tetragonium from Early Cretaceous (late Barremian-Aptian) Catefi ca locality, Portugal (S156369,
sample Catefi ca 382); SRXTM images showing reconstructed slice data of internal structure. Scale bars: Figs. 15, 23 (vertical scale at Fig. 15 ) = 0.5 mm;
Figs. 16 19 (vertical scale at Fig. 19 ) = 0.5 mm. Figs. 20 22 (vertical scale at Fig. 20) = 0.5 mm. Heavy gold coating seen as outer, light covering in Figs.
15 – 19, 23 . 15. Longitudinal section (LS) showing micropylar tube, micropylar canal, closure tissue, integument, and nucellus: note micropylar tube fi lled
with closure tissue and strongly adpressed to outer envelope. 16. Transverse section (TS) through tip of seed showing central micropylar canal formed by
the thin micropylar tube and surrounded by sclerenchyma of the envelope: at the apex, the micropylar tube consists of one cell layer (inner epidermis). 17.
TS below Fig. 16 showing the micropylar canal formed by the micropylar tube surrounded by sclerenchyma of the envelope: micropylar tube consists of
two cell layers (inner and outer epidermis). 18. TS below Fig. 17 (around the middle of the micropylar tube above the four valves of the seed envelope)
showing micropylar canal occluded by closure tissue: closure tissue comprised of radially elongate cells of inner epidermis of micropylar tube with several
additional outer cell layers (continuous with outer epidermis of Fig. 17 , see also Fig. 15 ). 19. TS near base of the micropylar tube below Fig. 18 showing
tips of the four valves of the seed envelope and closed micropylar canal. 20. LS of micropylar region showing seed envelope surrounding micropylar tube
with distinct inner epidermis and open micropylar canal that extends for most of its length (see Figs. 21, 22). 21. TS showing narrow, central micropylar
canal formed by the thin micropylar tube surrounded by sclerenchyma layer of the seed envelope: micropylar tube consisting of one cell layer (inner epi-
dermis). 22. TS below Fig. 21 showing narrow, central micropylar canal surrounded by the micropylar tube consisting of two cell layers (inner and outer
epidermis). 23. TS showing transition zone between inner and outer sclerenchyma layers of seed envelope.
258 American Journal of Botany [Vol. 96
chyma of the outer layer ( Figs. 12, 23 ). A transition zone of
partly open spaces between the inner and outer layer may indi-
cate an area of thin-walled cells that are not preserved. The outer
sclerenchyma layer has an inner zone of larger, radially extended
cells ( Figs. 10, 11 ) and an outer zone of smaller, more or less
isodiametric cells that are irregularly arranged ( Figs. 12, 13 ).
The outer sclerenchyma layer of the seed envelope is segmented
into four valves that are separated by the wing-like crests of the
inner layer ( Figs. 1, 2, 4 6, 9 ). The valves are elongated and
pointed at the apex. They also narrow toward the base ( Fig. 1 ).
The valves extend from the base of the seed to the base of the
micropylar region. In their apical part, the valves formed by the
outer sclerenchyma layer of the seed envelope are free from
the inner sclerenchyma layer ( Figs. 9, 19 ); otherwise, they are
more or less fused with the inner layer only separated by the partly
open spaces of the transition zone ( Figs. 10 14, 19, 23 ). The scler-
enchyma cells of the outer layer are shorter than those of the inner
layer and are irregular in shape and arrangement ( Figs. 12, 13 ).
Lobospermum gen. nov.
Derivation of generic name From the four-lobed shaped of
the seeds.
Generic diagnosis Seeds small, radially symmetrical, ellip-
soidal, micropylar region pointed; four-lobed in cross section.
Integument thin, micropylar tube long, narrow. Integument en-
closed by a seed envelope, except for the micropylar opening,
and attached to the envelope only at the base. Micropyle open
at the apex. Below, it is closed by a distinct, multicellular clo-
sure that fi lls the lower half of the micropyle. Micropylar clo-
sure formed mainly from a layer of larger cells that are expanded
radially toward the center of the micropylar tube. Seed lobes
separated by deep grooves; each with a narrow longitudinal me-
dian ridge. Inner surface of seed envelope smooth, nonpapillate;
outer surface smooth or rugulate. Seed envelope with an inner
apex of the nucellus are not well preserved. A megaspore mem-
brane has not been observed.
The seed envelope is formed from several layers of scleren-
chyma cells covered by an inner and outer cutinized epidermis.
The inner epidermis of the seed envelope consists of short, thin-
walled cells that are slightly longitudinally elongate and have a
smooth surface toward the inside of the seed ( Fig. 7 ). Cells
from the fi brous layer are seen as distinct transverse striations
under the epidermis ( Fig. 7 ). The inner epidermis of the seed
envelope is also smooth in the micropylar region and lacks pa-
pillae. The outer surface of the seed envelope is almost smooth
( Figs. 1 3, 8 ) with a thin cutinized epidermis of small, slightly
longitudinally elongate cells. In some seeds, the outer epider-
mis is almost intact and conceals the underlying valvate organi-
zation of the outer seed envelope ( Fig. 3 ).
The inner layer of the seed envelope is elongated at the apex
and is continuous around the integument. It is circular in cross
section near the apex where it surrounds the micropylar tube
( Figs. 8, 16, 17, 25 28 ), but it is four-angled below ( Figs. 4 6,
18 19, 27, 28 ). Close to the apex of the seed, the four corners of
the inner layer are extended into sharp, narrow, wing-like crests
( Fig. 5, 6, 11, 12, 19, 27, 28 ). In the body of the seed, they are
surrounded by and embedded in the outer sclerenchyma layer.
These crests can be traced from the base of the seed to the region
of the micropylar tube. They also extend radially to the outer
surface of the seed ( Figs. 4 6, 11, 12 ). Each wing-like crest has
a vascular bundle in its innermost part that extends from the
base to the apex ( Fig. 13 ). The sclerenchyma cells of the inner
layer are fi brous and arch upward in a chevron pattern ( Fig. 14 ).
The innermost fi bers are thin-walled, while the remaining fi ber
cells are thick-walled. The arches are short and the chevron pat-
tern forms shallow longitudinal ridges on the outside of the in-
ner layer. In cross section, these ridges are seen as a strongly
wavy outer line of demarcation ( Figs. 12, 23 ). The ridges on the
outside of the inner layer correspond to grooves in the scleren-
Figs. 24 28. Schematic line drawings through micropylar area of Buarcospermum tetragonium . Fig. 24. Longitudinal; Figs. 25 28, transverse sec-
tions. Yellow = integument; dark green = inner sclerenchyma layer of seed envelope; light green = outer sclerenchyma layer of the seed envelope. Figs.
25 28 at successively lower levels indicated with arrows on Fig. 24 . Scale bar Fig. 24 = 1 mm; Figs. 25 28 (at Fig. 28 ) = 0.5 mm. Compare with Figs.
95 – 98, 128 – 131 .
259
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
and outer sclerenchyma layer. Cells of inner sclerenchyma layer
long, fi brous arching upwards in a chevron pattern. Arches
formed by the fi bers are high and broad. Cells of outer scleren-
chyma layer narrow, longitudinally aligned. Inner and outer
sclerenchyma layers clearly delimited.
Type species Lobospermum stampanonii sp. nov.
Lobospermum stampanonii sp. nov. ( Figs. 29 – 44 )
Derivation of specifi c epithet In honor of Marco Stam-
panoni for his contribution to the development of X-ray micro-
tomography in paleontology.
Specifi c diagnosis — As for the genus with the following addi-
tions. Outer surface of seed almost smooth. Cells of outer scler-
enchyma layer of seed envelope equiaxial in transverse section.
Holotype — PP53375 from sample Puddledock 082, illus-
trated Figs. 29 – 33, 37 – 44 .
Paratype — PP53376 from sample Puddledock 082.
Type locality — Puddledock, Tarmac Lone Star Industries
sand and gravel pit, south of Richmond and east of the Appo-
mattox River, Prince George County, Virginia, USA
(37 ° 15 45 N, 77 ° 22 25 W).
Stratigraphic position and age of type stratum Basal part of
Subzone IIB, Potomac Group. Early Cretaceous (early or mid-
dle Albian).
Description and comments on the species The species is
based on a well-preserved isolated seed, ~3.8 mm long and 1.7
mm broad, as well as other seed fragments. The seed is radially
symmetrical and ellipsoidal in shape with a pointed apical mi-
cropylar region ( Figs. 29, 30 ). In cross section, the seeds are
four-lobed with deep grooves separating each lobe ( Figs. 29,
30, 32, 43, 44 ). Each lobe bears a median ridge ( Figs. 29, 30 )
that extends for the full length of the seeds or from the micro-
pylar area to about the middle of the seed ( Fig. 29 ).
The seeds are composed of a thin integument enclosed by an
outer sclerenchymatous envelope ( Figs. 30, 31, 37, 38, 40 ). The
integument extends apically into a long, narrow micropylar tube
( Figs. 31, 37 42 ). In the apical region, the micropylar tube consists
of a single layer of thin-walled cells, the inner epidermis ( Figs. 39,
40 ). Further down, an additional cell layer, the outer epidermis, is
developed. Toward the middle of the micropylar tube, the cells of
the inner epidermis extend radially to the center of the micropylar
canal, making the micropyle solid by completely closing the lower
half of the canal ( Figs. 37, 38, 41, 42 ). Below, the base of the mi-
cropyle the apex of the nucellus is poorly preserved.
The integument is enclosed by a robust envelope that is open
only at the apex ( Figs. 37, 38 ). Integument and seed envelope
are free from each other except at the base where the integu-
ment is broadly attached. The remains of tissues internal to the
integument are dense in this specimen, and their exact organi-
zation is not fully understood.
The seed envelope is formed from an inner and an outer scler-
enchyma layer. The inner epidermis of the seed envelope is
smooth and cutinized (Fig. 32). The inner epidermis is also
smooth where it surrounds the micropylar tube, and it lacks pa-
pillae ( Figs. 37, 38 ). The outer seed surface is almost smooth
with a thin cutinized epidermis. Sclerenchyma cells of the inner
layer are fi brous ( Figs. 34 36, 38, 43, 44 ) and prominently arched
forming a distinct chevron pattern ( Figs. 34, 35 ). The arches are
broad and high with only few arches over the entire width of the
seed. The fi brous layer is ~0.1 mm thick in most places, but thin-
ner under the grooves. The line of delimitation between the inner
brous layer and the outer layer of the envelope is sharp, and the
brous layer is easily detached. The outer layer consists mostly
of thin-walled, elongated sclerenchyma cells of equal width that
are aligned in distinct longitudinal rows ( Figs. 32 36 ). These
cells are equiaxial in transverse section. Over most of the seed,
the outer layer is three cells thick, but in the grooves there may
be only one or two layers of cells, while on the ridges there are
several layers of cells ( Figs. 34, 35 ). Vascular bundles extend
from base to apex along the line of the ridges ( Fig. 33 ).
Lobospermum glabrum sp. nov. ( Figs. 45 – 53 )
Derivation of the specifi c epithet — Referring to the smooth
surface of the seed.
Specifi c diagnosis — As for the genus with the following addi-
tions. Outer surface of seed almost smooth. Cells of outer scler-
enchyma layer not equiaxial in transverse section: cells toward
the inside distinctly taller, cells toward the outside equiaxial.
Holotype — S154554 from sample Famalic ã o 25, illustrated
Figs. 47, 48 .
Paratypes — S154553, S154555, S156005 – S156012 (sample
Famalic ã o 25).
Other specimens examined — S107690, S107691 (sample
Catefi ca 154), S156217, S156218 (sample Catefi ca 242),
S156220 – S156222 (sample Catefi ca 49).
Type locality — Famalic ã o, about 5 km SSE of Leiria, Portu-
gal (39 ° 42 16 N, 8 ° 46 12 W).
Stratigraphic position and age of type stratum Below Cal-
varia Member, Figueira da Foz Formation. Early Cretaceous
(late Aptian?).
Description and comments on the species All seeds are iso-
lated ( Figs. 45 49 ). They are ~2.3 4.8 mm long, and 1.5 2 mm
broad. The longest specimen is incomplete, and the inferred total
length is ~5.3 mm. Several fragmentary specimens consist only
of the inner fi brous layer shows the distinctive chevron pattern
( Figs. 51, 53 ). This layer is easily detached from outer layer. The
seeds are similar in general shape and organization to those of L.
stampanonii with a four-lobed morphology in cross section, lobes
separated by deep grooves, and an almost smooth to faintly ru-
gose outer surface ( Figs. 45 49 ). However, they differ in details
of the seed envelope. In L. glabrum , the median ridge of the lobes
is indistinct and extends for the full length of the seeds ( Figs.
45 – 48 ). In L. stampanonii , this ridge is more distinct but may
only extend part of the distance to the base of the seed. The orga-
nization of the seed envelope is also similar to that in L. stam-
panonii with the inner sclerenchyma layer formed from fi brous
cells arranged in a broad chevron pattern ( Figs. 51, 53 ) and cells
of the outer sclerenchyma layer narrow, elongate, and arranged in
longitudinal rows ( Fig. 52 ). However, the cells of the outer scler-
enchyma layer differ in being of unequal size in transverse sec-
tion with cells toward the inside being taller than the outer cells.
In one specimen, a distinct shiny substance covers the micropy-
lar opening and most of the apical region of the seed ( Figs. 45, 46 ).
260 American Journal of Botany [Vol. 96
Figs. 29 – 36. Lobospermum stampanonii from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; SEM images. Scale
bars: Figs. 29, 34 = 1 mm; Figs. 30, 32, 35 = 0.5 mm; Fig. 31, 36 = 0.2 mm; Fig. 33 = 0.2 mm. Figs. 29 33 . Holotype (PP53375, sample Puddledock 082).
Figs. 34 36 . Paratype (PP53376, sample Puddledock 082). 29. Lateral view of seed showing strongly lobed seed envelope. 30. Apical view showing mi-
cropylar area with seed envelope surrounding the micropylar tube. 31. Detail of micropylar area showing seed envelope and micropylar tube. 32. Outer
surface of seed envelope showing longitudinally aligned sclerenchyma and remains of thin cuticle of outer epidermis (white arrows). 33. Detail of outer
part of seed envelope showing the median vascular bundle of one lobe and pitted sclerenchyma. 34. Broken seed showing the anatomy of the seed envelope
with the arched fi brous inner layer and the longitudinally aligned sclerenchyma of outer layer. 35. Detail of inner and outer sclerenchyma layers of the seed
envelope. 36. Detail of seed envelope showing outer pitted sclerenchyma.
261
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Figs. 37 – 44. Lobospermum stampanonii from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; SRXTM images of
holotype (PP53375, sample Puddledock 082) showing reconstructed slice data of internal structure. Scale bars = 1 mm: Figs. 37, 38, 43, 44 (vertical scale
at Fig. 37 ); Figs. 39 42 (vertical scale at Fig. 40 ). 37. Longitudinal section (LS) through micropylar area showing micropylar tube, open micropylar canal,
and closure tissue, surrounded by apical part of seed envelope. 38. LS perpendicular to Fig. 37 showing details of the micropylar area and anatomy of seed
envelope. 39. Transverse section (TS) at seed apex showing central micropylar canal formed by the thin micropylar tube surrounded by sclerenchyma of
seed envelope. 40. TS through the micropylar area showing closure tissue comprised of integument cells partly expanded toward the center of the canal.
41. TS below Fig. 40 in the middle of micropylar tube showing the closure tissue mainly composed of radially extended cells. 42. TS below Fig. 41 near
base of micropylar tube showing degenerated cells near the center. 43. TS below the micropylar region in upper part of seed body showing the four-lobed
confi guration of the seed envelope with inner fi brous and outer smaller sclerenchyma cells. 44. TS below Fig. 43 near the middle of seed showing four-
lobed seed envelope comprised of two distinct layers of sclerenchyma.
262 American Journal of Botany [Vol. 96
Figs. 45 – 53. Lobospermum glabrum from the Early Cretaceous (late Aptian?) Famalic ã o locality, Portugal; SEM images. Scale bars: Figs. 45 49, 51 =
1 mm; Fig. 50 = 0.5 mm; Fig. 52 = 0.1 mm; Fig. 53 = 0.2 mm. Figs. 47 48 . Holotype (S154554, sample Famalic ã o 25). Figs. 45 – 46 . Paratype (S154553,
sample Famalic ã o 25). Figs. 49, 52 . Paratype (S154555, sample Famalic ã o 25). Fig. 50 . Paratype (S156005, sample Famalic ã o 25). Figs. 51, 53 . Paratype
263
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
(S156006, sample Famalic ã o 25). 45. Lateral view of seed showing the strongly lobed seed envelope, median ridges of the lobes, and remains of a secretion
in the micropylar area. 46. Apical view of seed in Fig. 45 showing lobes and remains of apical secretion. 47. Lateral view showing lobes and ridges of seed
envelope. 48. Apical view of seed in Fig. 47 showing lobes separated by deep grooves and apical micropylar region. 49. Broken seed with distinct grooves
between lobes showing cellular structure of seed envelope. 50. Apical part of seed showing outer epidermis of seed envelope. 51. Inner fi brous layer of seed
envelope showing chevron pattern formed by the arched fi bers. 52. Detail of outer part of seed envelope showing the median vascular bundle of one lobe
and pitted sclerenchyma. 53. Detail of the inner arched fi bers.
A similar covering has been observed in the same position in
other Lobospermum species, and the substance has the appearance
of a secretion. It is most likely the hardened remains of a polli-
nation droplet.
Lobospermum rugosum sp. nov. ( Figs. 54 – 57 )
Derivation of specifi c epithet Referring to the rugulate sur-
face of the seeds.
Specifi c diagnosis — As for the genus, with the following addi-
tions. Outer surface of seed rugulate. Cells of outer sclerenchyma
layer not equiaxial in transverse section: cells toward the outside
distinctly taller and forming the rugulate surface ornamentation.
Holotype — PP53374 from sample Puddledock 083, illus-
trated Fig. 55 .
Paratypes — PP53377 – PP53380, PP52705 – PP53708 (sample
Puddledock 082), PP53709 PP53710 (sample Puddledock 083).
Other specimens examined S156223 (sample Catefi ca
154), S156370 – S156371 (Catefi ca 358).
Type locality — Puddledock, Tarmac Lone Star Industries
sand and gravel pit, south of Richmond and east of the Appo-
mattox River, Prince George County, Virginia, USA
(37 ° 15 45 N, 77 ° 22 25 W).
Stratigraphic position and age of type stratum Basal part of
Subzone IIB, Potomac Group. Early Cretaceous (early or mid-
dle Albian).
Description and comments on the species All seeds are iso-
lated ( Figs. 54 56 ). They are ~3.7 4.1 mm long and 1.15 1.6
mm broad. Several specimens are fragmentary and consist only
of the inner fi brous layer with its distinct chevron pattern. This
inner layer is easily detached from outer layer. The seeds are
similar in general shape and organization to those of L. stam-
panonii and L. glabrum , with a robust outer seed envelope and
a thin integument that is extended apically into a long, narrow
micropylar tube. The micropylar canal is open apically ( Fig.
57 ). Lobospermum rugosum differs from the other two species
mainly in the rugulate external surface ornamentation of the en-
velope, which consists of irregular transverse ridges ( Figs. 54
56 ). In addition, the sclerenchyma cells of the outer layer of the
seed envelope are of unequal size in transverse sections. The
cells toward the outside are distinctly taller and form the rugu-
late ridges on the seed surface.
Rugonella gen. nov.
Derivation of generic name From the strongly rugulate sur-
face ornamentation of the seed envelope.
Generic diagnosis Seeds small, bilaterally symmetrical (with
a single axis of symmetry) and two lateral wings; nearly circular in
longitudinal outline in the broadest view, micropylar region slightly
pointed; shallowly triangular, three-lobed in cross section with
three grooves separating the lobes. Integument thin, micropylar
tube long, narrow. Integument enclosed by a seed envelope, except
for the micropylar opening, attached to the envelope only at the
base. Micropyle open at the apex. Below, micropylar closure
distinct, multicellular, with enlarged cells that extends toward the
center of the micropyle fi lling the lower half of micropylar tube.
Inner surface of seed envelope smooth, nonpapillate; outer surface
deeply rugulate, except on the wings. Seed envelope with an inner
and an outer layer of sclerenchyma. Cells of inner sclerenchyma
layer long, narrow and thin-walled, arching in a distinct chevron
pattern. Fiber arches broad and high. Cells of outer sclerenchyma
layer longitudinally aligned, narrow. Demarcation between inner
and outer sclerenchyma layers distinct.
Type species — Rugonella trigonospermum sp. nov.
Rugonella trigonospermum sp. nov. ( Figs. 58 – 71 )
Derivation of species epithet Referring to the triangular
shape of the seeds.
Specifi c diagnosis — As for the genus.
Holotype — PP53373 from sample Puddledock 083, illustrated
Figs. 58, 59, 61, 63, 64, 66 71 ).
Paratypes — PP53381-PP53383, PP53700 – PP53704 (sample
Puddledock 082), PP53698 PP53699 (sample Puddledock 083).
Type locality — Puddledock, Tarmac Lone Star Industries sand
and gravel pit, south of Richmond and east of the Appomattox
River, Prince George County, Virginia, USA (37 ° 15 45 N,
77 ° 22 25 W).
Stratigraphic position and age of type stratum Basal part of
Subzone IIB, Potomac Group. Early Cretaceous (early or mid-
dle Albian).
Description and comments on the species The species is
based on well-preserved isolated seeds, ~2.5 mm long and 2.3
mm broad. The seeds are bilaterally symmetrical and almost
circular in their broadest outline ( Fig. 58 ) with a short stalk in
some specimens. In cross section, the seeds are narrow triangu-
lar/three-lobed ( Figs. 58, 61, 69 71 ). The three lobes are un-
equal in size and differ in shape. The median, probably abaxial,
lobe is separated from the two lateral lobes by two deep grooves
( Figs. 58 61 ). It has a distinct, rounded ridge extending longi-
tudinally from the base to apex ( Figs. 58, 61, 70, 71 ). The two
lateral lobes are fl attened on one side, probably the ventral side,
and separated from each other by a shallow groove ( Figs. 61,
70, 71 ). They are extended laterally into a fl attened wing, ~0.4
mm wide, that forms the margin of the seed on either side ( Figs.
61, 63, 70, 71 ). The probable dorsal surface is strongly rugulate
and ornamented by irregular and transversely aligned ridges
264 American Journal of Botany [Vol. 96
Figs. 54 – 57. Lobospermum rugosum from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, U.S.A; SEM images. Scale
bars: Figs. 54 56 = 2 mm; Fig. 57 = 0.1 mm; Fig. 55 . Holotype (PP53374, sample Puddledock 083). Figs. 54, 57 . Paratype (PP53380, sample Puddledock
082). Fig. 56 . Paratype (PP53379, sample Puddledock 082). 54 56. Lateral view of three different seeds showing the lobed seed envelope, distinct median
ridges on the lobes, and transverse rugulate surface ornamentation. 57. Apical view showing the micropylar area with the seed envelope surrounding the
micropylar tube and micropylar canal.
( Figs. 58 60, 66 71 ). The probable ventral surface is smooth or
shallowly rugulate ( Figs. 61, 70, 71 ).
The seeds are composed of a thin integument enclosed by an
outer sclerenchyma envelope. The integument extends apically
into a long, narrow micropylar tube ( Figs. 60, 62, 64, 65, 67 ). In
the apical region of the micropyle, the integument consists of a
single layer of thin-walled cells. Toward the middle of the mi-
cropylar tube, there are several cell layers, including a layer of
enlarged cells that are radially extended toward the center of the
micropylar canal. These cells completely close the micropylar
canal ( Figs. 64, 65 ).
The integument is enclosed by a robust envelope that is open
only at the apex. Integument and seed envelope are free from
each other ( Figs. 67, 69 71 ) except at the base where the in-
tegument is broadly attached ( Fig. 67 ). The integument encloses
the nucellus. It is indistinct, but clearly free from the integu-
ment in the distal region ( Fig. 67 ). The tissues inside the integu-
ment are otherwise densely opaque, and a megaspore membrane
was not observed.
The seed envelope ( Fig. 67 ) is formed from an inner and an
outer sclerenchyma layer. The inner epidermis of the seed en-
velope is smooth, cutinized, and consists of thin-walled, nar-
row, longitudinally arranged cells. The inner epidermis is also
smooth around the micropylar tube and lacks papillae. The
outer seed surface has a thin cutinized epidermis ( Fig. 62 ).
The sclerenchyma cells of the inner layer are fi brous and
arched, forming a distinct chevron pattern ( Figs. 66 68 ). The
arches are broad and high with only a few arches over the entire
width of the seed. The delimitation between the fi brous layer
and the outer layer of the envelope is sharp, and the fi brous in-
ner layer is easily detached from the outer layer. The outer layer
is a few cell layers thick, consisting of small sclerenchyma cells
of unequal size. The outer cells are larger than the inner and
form the ridges on the surface of the envelope ( Figs. 66 68, 70,
71 ). The outer epidermis is thin and consists of small isodiamet-
ric cells arranged in longitudinal fi les ( Fig. 62 ), that sometimes
have a fi nely papillate surface ornamentation ( Fig. 63 ).
Lignierispermum gen. nov.
Derivation of generic name In honor of the French palaeo-
botanist Octave Lignier for his contribution to the understand-
ing of reproductive structures of Bennettitales.
Generic diagnosis — Seeds small, obovoid, micropylar re-
gion pointed; four-angled, slightly fl attened, bisymmetrical
(with two planes of symmetry) in cross section. Integument
thin, micropylar tube long, narrow. Integument enclosed by a
seed envelope, except for the micropylar opening, and at-
tached to the envelope only at the base. Nucellus thin, en-
closed by the integument; nucellus free distally, otherwise
fused to the integument. Micropyle open at the apex. Below,
micropylar closure distinct, multicellular, formed from sev-
eral cell layers fi lling the lower half of micropylar tube. Inner
surface of seed envelope smooth, nonpapillate; outer surface
smooth. Seed envelope sclerenchymatic comprising two dis-
tinct layers. Inner layer composed of transversely aligned fi -
ber cells; at the apical corners of the seed, the fi ber cells radiate
toward the outside to form four, narrow, wing-like, apically
pronounced crests. The outer layer is composed of radially
extended cells that increase in size toward the apex and
shorter, thin-walled cells covered by a distinct epidermis of
equiaxial cells. Four distinct longitudinal bundles extend in
the outer layer of the seed envelope from the seed base to
apex.
265
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Type species Lignierispermum maroneae sp. nov.
Lignierispermum maroneae sp. nov. ( Figs. 72 – 98 )
Derivation of specifi c epithet — In honor of Federica Marone in
appreciation of her support in the X-ray microtomographic studies.
Specifi c diagnosis — As for the genus.
Holotype — PP53214 from sample Puddledock 082, illus-
trated Figs. 72 – 77, 8294 .
Other specimens examined — S156219 (sample Catefi ca 49).
Type locality — Puddledock, Tarmac Lone Star Industries
sand and gravel pit, south of Richmond and east of the Appo-
Figs. 58 – 65. Rugonella trigonospermum from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; SEM images. Scale
bars: Figs. 58 61 = 1 mm; Fig. 62 = 0.2 mm; Fig. 63 = 0.5 mm; Fig. 64 = 0.05 mm; Fig. 65 = 0.025 mm. Figs. 58, 59, 61, 63, 64 . Holotype (PP53373,
sample Puddledock 083). Figs. 60, 62, 65 . Paratype (PP53382, sample Puddledock 082). 58. Dorsiventral view of seed showing the lobed seed envelope,
lateral wings, and transverse, rugulate surface ornamentation. 59. Lateral view. 60. Dorsiventral view showing seed envelope split at apex exposing micro-
pylar tube. 61. Apical view showing the bilaterally symmetrical, triangular shape of the seed envelope and fl at lateral wings. 62. Detail of seed in Fig. 60
showing micropylar tube. 63. Outer surface of seed envelope showing outer papillate epidermis and transverse ridges. 64. Detail of micropylar area showing
outer epidermal cells of micropylar tube and inner closure tissue surrounded by sclerenchyma of seed envelope. 65. Apical view of micropyle in Figs. 60,
62 , showing outer epidermis of micropylar tube and closing tissue.
266 American Journal of Botany [Vol. 96
267
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
ment encloses the nucellus ( Figs. 82, 83, 88 92 ). The nucellus
membrane is poorly developed. It is fused to the integument
except apically where it is free ( Fig. 82 ). Tissues internal to the
integument are generally crushed and not easy to interpret. A
megaspore membrane was not observed.
The seed envelope has a distinct outer and inner epidermis.
The inner epidermis consists of short, thin-walled cells that
have a smooth surface toward the inside of the seed. It is dis-
tinct in the micropylar region where it forms a ring of small,
nonpapillate and equiaxial cells ( Fig. 84 ). The outer seed sur-
face is almost smooth ( Figs. 72, 73, 78, 82 ) with a thick cuti-
nized epidermis of small, slightly transversely elongate cells
and with scattered swellings ( Figs. 77, 80, 81 ). These swell-
ings are most abundant in the upper part of the seed. They are
either cushion-shaped or more elongated. The elongated
structures are always broken, and the rounded structures are
often broken. The bases appear to be formed from several
cells. These elongated or cushion-shaped structures are prob-
ably short trichomes or papillae and are similar to epidermal
papillae or trichome bases recorded for Bennettitales ( Harris,
1969 ; Watson and Sincock, 1992 ; Pott et al., 2007 ). Just be-
low the micropylar projection, the outer epidermis has a ring
of regularly spaced hollows in the cuticle of the seed envelope
( Figs. 72 74, 76 ) that may be damaged stomata or burst se-
cretory cells.
The seed envelope consists of two layers. The inner layer
of the seed envelope is continuous around the integument
and also surrounds the micropylar tube. It consists of trans-
versely aligned fi ber cells. Near the apex, the fi ber layer
projects into the corners of seed envelope to form four, nar-
row, wing-like crests that extend almost to the surface of the
envelope ( Figs. 87 92 ). The outer layer consists of one layer
of thick-walled and strongly pitted sclerenchyma cells that
are arranged in a radiating pattern. Subapically, these cells
are strongly expanded and make up most of the wall of the
seed envelope ( Figs. 82, 83, 87 ). Toward the outside, the
outer layer of the seed envelope comprises a thin layer of
smaller, thin-walled cells that are covered by the outer epi-
dermis ( Figs. 83, 86 ). Four vascular bundles extend immedi-
ately below this layer from the base to apex ( Figs. 92, 94 )
and are seen as four longitudinal ridges on the seed surface
( Figs. 72 74 ). Four additional vascular bundles are present
in the outer layer at the base of the seed. These bundles oc-
cur between the four major bundles and extend for ~0.5 mm
and give the base of the seed an octangular shape in trans-
verse section ( Figs. 93, 94 ).
Recognition of new genera and species The four new
genera of fossil seeds described here are linked by the com-
mon organizational ground plan of having the integument
enclosed by an angular, sclerenchymatous seed envelope
( Table 1 ). Buarcospermum , Lobospermum , and Rugonella
are further linked by having fi ber cells arranged in a distinct
chevron pattern in the inner part of the seed envelope. In
mattox River, Prince George County, Virginia, USA
(37 ° 15 45 N, 77 ° 22 25 W).
Stratigraphic position and age of type stratum Basal part of
Subzone IIB, Potomac Group. Early Cretaceous (early or mid-
dle Albian).
Description and comments on the species Lignierisper-
mum maroneae is based on a single, well-preserved, isolated
seed from the Puddledock locality, USA ( Figs. 72 75, 82
94 ), and one well-preserved isolated seed from the Catefi ca
locality, Portugal ( Figs. 78 81 ). The Catefi ca seed is slightly
larger than the Puddledock specimen and broader in shape.
They are treated here as one species because of the close
similarity in general shape and structure and identical epi-
dermal features.
The seeds are small. The Puddledock specimen is ~2.7 mm
long and up to 1.3 mm broad. The Catefi ca specimen is ~3.1
mm long and 1.7 mm in maximum width but is broken proxi-
mally, and the complete length is not known. Both the Puddle-
dock and the Catefi ca seeds are bisymmetrical and obovoid
( Figs. 72 74, 78, 82 ). The Puddledock specimen is narrower
than the Catefi ca specimen. It tapers proximally into a pointed
base and is truncate near the apex with a central projecting mi-
cropylar area ( Figs. 72, 73, 82, 83 ). In transverse section, the
seeds are four-angled for most of their length ( Figs. 87 92 ).
Close to the base, four additional low ridges give the seed an
octangular transverse section ( Fig. 93, 94 ).
The X-ray microtomography of the holotype shows that the
seed is composed of a thin integument enclosed by a scleren-
chymatous seed envelope ( Figs. 82 94 ). The integument is ex-
tended apically into a long, narrow micropylar tube, ~0.36 mm
long and 0.07 mm wide ( Figs. 82, 83 ). In the apical region, the
micropylar tube consists of a single layer of thin-walled cells,
the inner epidermis, that forms a circular ring around the open
micropylar tube ( Figs. 75, 83, 84 ). Further down, an additional
cell layer, the outer epidermis, is formed ( Figs. 83, 85 ). Toward
the middle of the micropylar tube, the inner epidermal cells ex-
pand and radiate to the center of the micropylar canal, closing
the canal completely ( Figs. 82, 83, 87 ). In the closure area, the
central cells become indistinct, and at this level the micropylar
tube is strongly adpressed to the seed envelope so that the two
tissues are diffi cult to distinguish from each other ( Figs. 82, 83, 87 ).
At the base of the micropylar tube, the integument and seed
envelope are again distinct from each other as in the apex. Also
at the base of the micropylar tube, the cells of the integument
become larger ( Fig. 83 ), and the micropylar canal is at this level
distinguished as a narrow, star-shaped opening ( Fig. 87 ). The
different tissues of the micropylar region are illustrated dia-
grammatically ( Figs. 95 – 98 ).
The integument is surrounded by a robust envelope that is
open only at the apex ( Figs. 72 76, 78, 79, 82 94 ). Integument
and seed envelope are free from each other except at the base
where the integument is broadly attached ( Fig. 82 ). The integu-
Figs. 66 – 71. Rugonella trigonospermum from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; SRXTM images of
holotype (PP53373, sample Puddledock 083) showing reconstructed slice data of internal structure. Scale bar Figs. 66 68 (vertical at Fig. 66 ) = 1 mm;
67 71 (horizontal at Fig. 70 ) = 1 mm. 66. Longitudinal section (LS) through lobes showing cellular structure of seed envelope and internal tissue. 67. LS
perpendicular to section in Fig. 66 showing details of the micropylar area and seed envelope. 68. LS (tangential) of sclerenchyma of seed envelope showing
brous inner layer and shorter outer cells. 69. Transverse section (TS) at apex of the seed showing central micropylar tube surrounded by the triangular seed
envelope. 70. TS through seed below micropylar area showing integument free from the seed envelope. 71. TS near middle of the seed showing three-lobed
seed envelope composed of two distinct layers of sclerenchyma.
268 American Journal of Botany [Vol. 96
269
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Lignierispermum , the inner fi bers are straight, transversely
aligned and do not form a chevron pattern or arches. Buar-
cospermum and Lobospermum both have radially symmetri-
cal four-angled seeds. Seeds of Rugonella are bilaterally
symmetrical (single plane of symmetry) and three-angled,
and Lignierispermum is four-angled but slightly fl attened and
bisymmetrical (two planes of symmetry). In Lobospermum
and Rugonella , the fi bers of the inner sclerenchyma layer
form only a few broad arches over the entire width of the
seed, while in Buarcospermum the arches are many, short
and closely spaced. Seeds of Buarcospermum are clearly dis-
tinguished from those of both Lobospermum and Rugonella
by division of the seed envelope into an inner winged part
and an outer four-valved part.
Buarcospermum and Lignierispermum both have four apical
wing-like crests that project from the fi brous inner layer of the
seed envelope. They also both have radiating sclerenchyma
cells toward the outside of the seed envelope, but in Lignieri-
spermum these cells are strongly extended near the apex and
form most of the wall at this level of the seed envelope. Lignieri-
spermum and Buarcospermum differ from the two other genera
in having much longer micropylar tubes. Closure of the micro-
pyle in all genera is mainly by the enlarged cells of the inner
epidermis of the integument that extend radially into the center
of the micropylar canal ( Table 1 ).
The different species of Lobospermum are distinguished by
differences in size, shape and cellular structure as well as orna-
mentation of the envelope ( Table 1 ). Seeds of L. rugosum have
a rugulate outer surface and are generally more slender than
those of L. stampanonii and L. glabrum . Lobospermum rugosum
is similar to L. glabrum in having a median ridge on the lobes
that is indistinct and extends for the full length of the seeds. The
seed envelope is generally thinner than in L. stampanonii .
DISCUSSION
Phylogenetic position of Buarcospermum, Lignierisper-
mum, Lobospermum, and Rugonella Seeds that are orga-
nized in the same way as those of Buarcospermum ,
Lignierispermum , Lobospermum , and Rugonella are known
only for members of two extinct orders of seed plants, Bennet-
titales and Erdtmanithecales, as well as for extinct and extant
Gnetales. The same organization is also seen in several iso-
lated seeds recognized in Early Cretaceous mesofossil fl oras
from Denmark (Bornholm), Portugal, and eastern North Amer-
ica that remain to be described in detail (E. M. Friis, K. R.
Pedersen and P. R. Crane, work in progress). These isolated
mesofossils also include the small four-angled seeds ( square
seeds ) discussed recently by Friis et al. (2007) and other simi-
lar forms.
The seeds of these various groups of plants differ in certain
structural details, but they are all linked by strong similarities
in their unusual organization and anatomy. All have a thin
membranous integument extended into a long micropylar tube,
and the integument is tightly enclosed by one or two seed en-
velopes, which are open only apically where there is access to
the micropylar tube. Most of these fossil seeds are three- or
four-angled in cross section, but more rarely there are also
two-angled forms, as well as fi ve- and six-angled forms in
some Bennettitales ( Stopes, 1918 ). A further consistent fea-
ture of the seeds in the groups listed is that the apical part of
the micropyle consists of only a single layer of integument
cells that form a tube around the open micropylar canal. At the
apex, the micropylar canal is hollow and circular in cross sec-
tion, but below it is closed by a distinct closure mechanism
involving either expansion of the integument into the micro-
pylar canal or a mucilaginous secretion. Details of the cellular
closure mechanism of the micropylar canal differ among the
different seed types, but the closure is mainly by the cells of
the inner epidermis of the integument that extend radially into
the center of the micropylar canal. The nucellus is free from
the integument apically, but fused to the integument farther
down. The nucellus is often somewhat crushed, and none of
the seeds exhibit a distinct pollen chamber. A megaspore
membrane has currently not been observed in any of the stud-
ied seeds. It was probably either poorly developed or lacking
as in extant Gnetales.
A phylogenetic analysis that included the small square
seeds and Erdtmanithecales in the seed plant matrix of Hilton
and Bateman (2006) placed both taxa in a clade that also in-
cludes Bennettitales and Gnetales ( Friis et al., 2007 ). Buar-
cospermum , Lignierispermum , Lobospermum , and Rugonella,
as well as the other isolated seeds considered here, have the
same combination of characters as the square seeds of Friis et
al. (2007) and are resolved as part of the same group. In these
analyses this clade, referred to as the Bennettitales-Erdtmanith-
ecales-Gnetales (BEG) group, is united by the common ovule/
seed organization outlined above, as well as by paracytic sto-
mata and tectate pollen grains with a granular infratectal layer
( Friis et al., 2007 ). While this hypothesis needs to be tested by
a new generation of more rigorous phylogenetic analyses of liv-
ing and fossil seed plants, the evidence presented here provides
further support for this grouping by further documenting clear
structural similarities between the seeds of Buarcospermum,
Lignierispermum , Lobospermum , and Rugonella, and those of
Bennettitales, Erdtmanithecales, and Gnetales.
Buarcospermum, Lignierispermum, Lobospermum, Rugo-
nella, and other isolated seeds Currently, more than 20
different seed types with the same common organizational
ground plan seen in Buarcospermum , Lignierispermum ,
Figs. 72 – 81. Figs. 72 – 77 . Lignierispermum maroneae from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; holo-
type (PP53214 sample Puddledock 082). Figs. 78 81 . Lignierispermum maroneae from the Early Cretaceous (late Barremian-Aptian) Catefi ca locality,
Portugal; (S156219 sample Catefi ca 49). SEM images; Scale bars: Figs. 72, 73, 78 = 1 mm; Fig. 74 = 0.5 mm; Fig. 75, 80 = 0.1 mm; Fig. 76, 79 = 0.25
mm; Fig. 77, 81 = 0.2 mm. 72, 73. Lateral views showing seed envelope with four longitudinal ribs, projecting micropylar area and ring of ruptured cells
immediately below. 74. Apical view showing the four-angled outline, outer epidermis of seed envelope and ring of ruptured cells toward the apex. 75.
Micropylar area in apical view showing the micropylar tube and open micropylar canal surrounded by the sclerenchyma cells of the seed envelope. 76.
Lateral view of seed apex showing outer epidermis of seed envelope and ring of ruptured cells. 77. Outer surface of seed envelope showing epidermis with
transversely elongate cells and scattered papillae/trichome bases. 78. Lateral view of seed showing longitudinal ribs, micropylar area, and transversely
elongate epidermal cells. 79. Lateral view of seed apex showing epidermal features near micropyle. 80. Epidermis of seed envelope with broken papilla/
trichome. 81. Outer surface of seed envelope showing rows of transversely elongate epidermal cells and scattered papillae/trichomes.
270 American Journal of Botany [Vol. 96
271
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Lobospermum , and Rugonella have been recognized among
Early Cretaceous mesofossils ( Figs. 99 121 ). Some have been
assigned to Gnetales (species of Ephedra and Ephedrisper-
mum , Rydin et al., 2006a ; discussed later) or to Erdtmanithe-
cales (species of Erdtmanispermum , Pedersen et al., 1989b ,
Mendes et al., 2008b ; discussed later), but most are currently
unassigned within the BEG group and remain to be formally
named. Especially common and widespread are small four-
angled seeds ( square seeds ) very similar to those described
and illustrated recently ( Friis et al., 2007 ). Seeds of this gen-
eral kind occur in most of the Early Cretaceous fl oras that we
have sampled in Portugal and eastern North America, which
range in age from late Barremian/early Aptian to early/middle
Albian. They all exhibit the same basic morphology with four
distinct angles and a surface ornamentation of irregular trans-
verse ridges. However, they also vary considerably in certain
details. Some have pointed structures that extend upward from
the apical corners of the seeds and superfi cially resemble te-
pals of epigynous angiosperm fl owers ( Figs. 109, 110, 122
124, 126, 127 ), while others apparently lack these structures
( Fig. 125 ) . There is also variation in structural details of the
seed envelope. Some have radially extended cells in the apical
region of the seeds. The magnitude of variation indicates that
these small square seeds comprise several different species,
but they perhaps should also be separated into more than one
genus. Further detailed studies of specimens from different
localities of different ages, are needed before the limits of
genera and species become clear and before these seeds can be
formally named.
The square seeds are similar to those of Lobospermum and
Rugonella in having a rugulate surface pattern of irregular,
transverse ridges. In Lobospermum , these ridges are only pro-
nounced in L. rugosum. They are faintly developed in L. stam-
panonii and very faint in L. glabrum . Lobospermum stampanonii,
Rugonella , and the square seeds also have a similar closure of
the micropylar canal by radially expanded cells of the integu-
ment that block the micropylar canal.
Lobospermum and Rugonella differ from the square seeds
in having arched fi bers forming a chevron pattern in the inner
sclerenchyma of the seed envelope. Rugonella is also distin-
guished by its bilaterally symmetrical, triangular shape. Seeds
of Buarcospermum are distinguished from the square seeds
in having a smooth outer surface of the seed envelope and
arched fi ber cells. In the anatomy of the seed wall, the square
seeds are more similar to Lignierispermum in having trans-
versely aligned inner fi bers. Otherwise, the square seeds are
distinguished from all four genera by their tepal-like apical ex-
tensions ( Figs. 122 124, 126, 127 ).
Also part of this same complex of isolated gymnosperm
seeds is Raunsgaardispermum lusitanicum Mendes, Pais et
Friis ( Figs. 99, 100 ), recently described from the earliest Cre-
taceous of Portugal ( Mendes et al., 2008a ). Raunsgaardisper-
mum Mendes, Pais et Friis is clearly similar to Buarcospermum ,
Lignierispermum , Lobospermum , and Rugonella in its overall
organization, with a thin inner integument extended into a long
micropylar tube surrounded by a sclerenchymatous envelope.
However, Raunsgaardispermum differs from the other seeds
in having an envelope with two valves, rather than three or
four, and in the presence of narrow longitudinal ribs with dis-
tinct bifurcations. Raunsgaardispermum is distinguished from
Buarcospermum , Lignierispermum , Lobospermum , and Rugo-
nella, but linked to Ephedra (Gnetales), by the presence of pa-
pillae on the inner surface of the seed envelope surrounding
the micropylar tube. However, it is distinguished from Ephe-
dra by its nonephedroid pollen. The pollen grains of Raun-
sgaardispermum are monocolpate and psilate-punctate; more
similar to those of Bennettitales ( Mendes et al., 2008a ). Unfor-
tunately, the pollen grains of Buarcospermum , Lignierisper-
mum , Lobospermum , Rugonella , and the “ square seeds ” are
not yet known.
Buarcospermum, Lignierispermum, Lobospermum, Rugo-
nella, and seeds of Gnetales Extant Gnetales include three
genera, Ephedra L., Welwitschia Hook. f., and Gnetum L.,
which are relicts of a formerly much more diverse and widely
distributed group (e.g., Rydin et al., 2006a ). In the fossil record,
Gnetales are particularly well represented and diverse in Early
Cretaceous fl oras. Until recently, the group was mainly repre-
sented by distinctive polyplicate Ephedra -type pollen ( Crane
and Lidgard, 1989 ), but over the past few years the macro- and
mesofossil record of Gnetales has expanded considerably. Es-
pecially important are compressions/impressions of Ephedra -
like shoots and branching systems with attached leaves and
reproductive structures from the Early Cretaceous Yixian For-
mation. These include species assigned to Liaoxia Cao et S. Q.
Wu (e.g., Rydin et al., 2006b ), Ephedrites G ö ppert et Berendt
(e.g., Sun et al., 2001 ) or Ephedra (e.g., Yang et al., 2005 ).
Another probable gnetalean fossil from the Yixian Formation is
Gurvanella dictyoptera Krassilov. Gurvanella Krassilov was
rst described from the Early Cretaceous of Mongolia based on
isolated winged seeds ( Krassilov, 1982 ), but was later recog-
nized also in the Yixian Formation where it is known from
branching systems bearing both leaves and seeds (fi rst described
as Chaoyangia Duan, 1998 ; Wu, 1999 ; Sun et al., 2001 ). De-
tails of the ovulate structures are unclear and are preserved only
as impressions/compressions. However, the branching systems
on which the seeds are borne are similar to those of other ephed-
roid plants from the same strata.
Compression/impression ephedroid fossils are also known
from the Early Cretaceous of the Lake Baikal area ( Eoantha
Figs. 82 – 87. Lignierispermum maroneae from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; SRXTM images of
holotype (PP53214, sample Puddledock 082) showing reconstructed slice data of internal structure. Figs. 82, 83, 86 . Longitudinal sections. Figs. 84 85,
87 ). Transverse sections. Scale bars: Fig. 82, 83 = 1 mm; Figs. 84, 85, 87 (vertical scale at 85) = 0.5 mm; Fig. 86 = 0.25 mm. 82. Longitudinal section (LS)
through micropylar area of seed showing micropylar tube, micropylar canal, closure tissue, integument with basal attachment, nucellus, and sclerenchyma
of seed envelope. 83. Detail of micropylar region showing integument extended into micropylar tube that is open apically and closed in the middle: note
radially expanded cells in the subapical region of the seed envelope. 84. Transverse section (TS) through the tip of seed showing central micropylar canal
formed by the thin micropylar tube and surrounded by sclerenchyma of the seed envelope: micropylar tube consisting of one cell layer (inner epidermis),
seed envelope with a distinct inner epidermis and smooth inner surface. 85. TS through the micropylar area below Fig. 84 showing micropylar tube with
an additional cell layer (outer epidermis). 86. LS of seed envelope showing inner transverse fi bers, outer sclerenchyma cells and outer epidermis. 87. TS
near base of micropylar tube showing the micropylar closure with narrow star-shaped opening; seed envelope showing radially extended cells of outer
sclerenchyma layer and four crest-like extensions of inner sclerenchyma layer.
272 American Journal of Botany [Vol. 96
273
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
zherikhinii Krassilov [1986] ), the Potomac Group sequence
( Drewria potomacensis Crane et Upchurch [1987] ) and from
the Early Cretaceous Crato Formation of Brazil ( Mohr et al.,
2007 ). The Crato Formation has also yielded macrofossils re-
lated to Welwitschia ( Rydin et al., 2003 ; Dilcher et al., 2005 ;
Mohr et al., 2007 ). Eoantha Krassilov is especially signifi cant
because the seeds contain ephedroid pollen in the micropyle.
Drewria Crane et Upchurch is important because it is a small
plant with opposite and decussate laminar leaves that have ve-
nation similar to that in cotyledons of Welwitschia .
All extant genera of Gnetales have seeds consisting of a nu-
cellus enclosed by a thin, membranous integument and one
( Ephedra , Welwitschia ) or two ( Gnetum ) additional seed enve-
lopes ( Martens, 1971 ). The nucellus is fused to the integument
for part of its length, but the integument is free from the seed
envelope except at the base where it is broadly attached. The
apical cells of the nucellus disintegrate to form an indistinct pol-
len chamber ( Martens, 1971 ), and a megaspore membrane is
thin ( Ephedra , Welwitschia ) or lacking ( Gnetum ) ( Crane, 1985 )
At the apex, the integument is elongated into a long, narrow
micropylar tube that projects well beyond the seed envelope.
The apex of the micropylar tube is irregular and lobed to various
degrees. It is strongly lobed in Gnetum (e.g., Takaso and Bou-
man, 1986 ), less so in Ephedra (e.g., Yang, 2007 ), and modifi ed
into a prominent funnel in pollen-producing owers ” of Wel-
witschia . In Gnetum , at the time of pollination, the outer cells of
the micropylar tube divide to form a distinct umbrella-like
ange ( Berridge, 1911 ; Martens, 1971 ). After pollen grains
have entered the ovule, the micropylar canal is closed, either by
a hardened mucilaginous secretion ( Ephedra , Thoday and Ber-
ridge, 1912 ) or by periclinal divisions and radial extensions of
the cells in the middle and proximal part of the micropylar tube
( Gnetum and Welwitschia , Berridge, 1911 ). Toward the base,
the central cells of the closure tissue in Welwitschia and Gnetum
degenerate to form an irregular central cavity ( Berridge, 1911 ).
In extant Ephedra, the single seed envelope is usually bilat-
erally symmetrical or triangular. More rarely, it is four-angled.
In Early Cretaceous Ephedra , the seed envelope is usually four-
angled ( Rydin et al., 2006a ). Internally, the envelope is dis-
tinctly sclerenchymatous, although sometimes fl eshy externally.
The outer surface is usually smooth, but in some species such as
E. rhytidosperma (e.g., Yang, 2007 ), it is ornamented by irregu-
lar transverse ridges. The inner surface of the seed envelope is
smooth except around the micropylar tube where it is distinctly
papillate.
In seeds of Gnetum, the inner (fi rst) seed envelope is usually
free from the integument except at the base where it is broadly
attached. Sometimes the two layers are fused for part of their
length ( Takaso and Bouman, 1986 ). The inner seed envelope
has an inner sclerenchymatous layer of longitudinally elongate
ber cells, followed by a layer of sclerenchyma cells that are
elongated radially and an outermost layer of thin-walled, more
or less isodiametric cells ( Quisumbing, 1925 ). The middle layer
of radiating cells is particularly well developed in the subapical
region ( Fig. 128 ) and is sometimes missing farther down (e.g.,
Gnetum montanum Markgraf described by Rodin and Kapil,
1969 ). The outer (second) seed envelope is fl eshy, with abun-
dant lactifers as well as scattered sclereids and fi bers ( Rodin
and Kapil, 1969 ).
Seeds of Welwitschia differ from those of Ephedra and Gne-
tum (and other taxa in the BEG group) in lacking the robust
sclerenchyma layer in the seed envelope. Instead, the seed en-
velope forms a pronounced fl attened, membranous, papery
wing ( Martens, 1971 ). The fi bers of the wing are arranged in a
distinct chevron-like pattern reminiscent of that in Buarcosper-
mum , Lobospermum , and Rugonella ( Martens, 1971 ). This fea-
ture is not seen in the seed envelope of Ephedra and Gnetum .
Recent investigations of mesofossil fl oras from the Early
Cretaceous have recognized small fossil seeds very similar to
those of extant Ephedra . In Ephedra portugallica Rydin, Ped-
ersen, Crane et Friis from the Early Cretaceous (late Aptian or
early Albian) of Buarcos, Portugal, and Ephedra drewriensis
Rydin, Pedersen, Crane et Friis ( Figs. 107, 108 ) from the Early
Cretaceous (early Aptian) of Drewry s Bluff, Virginia, USA,
the seed envelope is four-angled ( Rydin et al., 2006a ). As in
some species of extant Ephedra (e.g., E. rhytidosperma ), the
surface of the sclerenchymatous tissue in the outer seed enve-
lope is sometimes ornamented by irregular, transverse ridges.
In both species, distinctive polyplicate pollen grains, very simi-
lar to those of extant Ephedra, occur in the micropyles. Ephe-
dra drewriensis occurs at the same locality as Drewria
potomacensis , although at a slightly different stratigraphic
level.
Dispersed fossil seeds assigned to Ephedrispermum lusitani-
cum ( Figs. 107, 108 ) from the Early Cretaceous (late Aptian or
early Albian) of Buarcos, Portugal, differ from those assigned
to Ephedra in the absence of papillae on the inner surface of the
envelope and the crosswise pattern of sclerenchyma cells that
comprise the hard inner layer of the envelope. However, these
seeds also have distinctive Ephedra -like pollen in the micro-
pyle ( Rydin et al., 2006a ).
In addition to the three species of fossil ephedroid seed al-
ready formally described, there are also a variety of other seeds
from the Early Cretaceous of eastern North America and Portu-
gal that are probably related to Ephedra (e.g., Fig. 7 in Rydin et
al., 2006a ). These are all of similar construction to the fossil
seeds of Ephedra and Ephedrispermum with a more or less an-
gular sclerenchymatous envelope. At least one of these seeds
has ephedroid pollen in the micropyle.
Buarcospermum , Lignierispermum , Lobospermum , and
Rugonella are similar to seeds of Gnetales in their general or-
ganization (see above), but they differ in structural details.
Lobospermum rugosum and Rugonella are particularly similar
to the seeds of some Ephedra species (e.g., E. rhytidosperma)
in having a rugulate surface pattern of irregular transverse
ridges. This confi guration is also reminiscent of that in seeds
of Eoantha zherikhinii ( Krassilov, 1986 ), which contain
ephedroid pollen.
Seeds of Ephedra are similar to those of Buarcospermum ,
Lignierispermum , Lobospermum , and Rugonella in having
Figs. 88 – 94. Lignierispermum maroneae from the Early Cretaceous (early or middle Albian) Puddledock locality, Virginia, USA; SRXTM images of
holotype (PP53214, sample Puddledock 082) showing reconstructed slice data of internal structure. Successive transverse sections from near apex to base.
Scale bar = 1 mm. 88. Transverse section (TS) near base of micropylar tube showing wing-like crests and radiating sclerenchyma cells of the seed envelope:
note thick-walled cells of the integument. 89. TS below the micropylar region showing seed envelope, integument and apex of nucellus. 90 94. Sections to
base of seed showing decreasing size of radiating sclerenchyma cells: note four vascular bundles in the corners of seed in Fig. 92 , eight vascular bundles
in Figs. 93, 94 .
274 American Journal of Botany [Vol. 96
granular infratectal layer. Eucommiidites ranges from the Early
Jurassic to the Late Cretaceous.
Several different microsporangiate structures with Eucommi-
idites pollen in situ have been identifi ed from the Cretaceous
including Erdtmanitheca texensis Pedersen, Crane et Friis
(1989b) , Eucommiitheca hirsuta Friis et Pedersen (1996), and
Bayeritheca hughesii Kva č ek et Pacltov á (2001) . Eucommiid-
ites pollen grains have also been discovered in situ in the micro-
pyles of several different kinds of seeds from the Early
Cretaceous. These seeds are all isolated and include Erdtmani-
spermum balticum Pedersen, Crane et Friis from Bornholm,
Denmark ( Pedersen et al., 1989b ) ( Figs. 101, 102 ), Erdtmani-
spermum juncalensis Mendes, Friis & Pais from Portugal
(2008b), Spermatites pattensis Hughes from southern England
( Hughes, 1961 ), and Spermatites patuxensis Brenner from east-
ern North America ( Brenner, 1967 ).
Seeds of Erdtmanithecales assigned to Spermatites, studied
as macerations, clearly show an integument with a long, narrow
micropylar tube containing Eucommiidites pollen, and a
seed envelope surrounding the integument. Seeds assigned to
Erdtmanispermum are lignitic and have cuticles as well as other
tissues preserved. They consist of a robust seed envelope en-
closing a membranous integument that extends apically into a
long narrow micropylar tube. The tube extends beyond the seed
envelope. The seed envelope is sclerenchymatous, distinctly
three-parted, and sometimes splits into three valves. The inner
surface of the seed envelope is smooth, including where it sur-
rounds the micropylar tube. The outer surface is smooth or
sometimes slightly rugulate with irregular transverse ridges
( Mendes et al., 2008b ).
Seeds of Erdtmanithecales are similar in general structure to
those of Buarcospermum , Lignierispermum , Lobospermum ,
and Rugonella. Like Erdtmanispermum , seeds of these four
genera lack the papillate lining around the micropylar tube.
However, Erdtmanispermum seeds are distinguished from
Buarcospermum , Lignierispermum , and Lobospermum in their
constant triangular form and from the triangular seeds of Rugo-
nella by their radial (rather than bilateral) symmetry and lack of
wings ( Figs. 101, 112 ). Seeds of Erdtmanithecales are further
distinguished from Buarcospermum , Lobospermum , and Rugo-
four-angled and three-angled forms in different taxa. However,
the seeds of all four fossil genera are clearly distinguished from
those of Ephedra in having cellular closure of the micropylar
canal. This contrasts with the hardened mucilaginous secretion
that closes the micropyle of Ephedra . In details of the micropy-
lar closure, the new fossil genera are more similar to both Wel-
witschia and Gnetum . The four new genera are further
distinguished from Ephedra by the absence of a papillate lining
on the seed envelope surrounding the micropylar tube. Seeds of
Ephedra (and Gnetum ) also lack the arched chevron arrange-
ment of fi bers seen in Buarcospermum , Lobospermum , Rugo-
nella , and extant Welwitschia .
The outer fl eshy (second) seed envelope, seen in seeds of
Gnetum , has not so far been observed for any of the isolated
seeds. This could perhaps be due to the lower fossilization
potential of parenchymatous tissue, but in the absence of any
remains of an outer tissue we assume that the fossils had
only a single seed envelope. Gnetum is also distinguished
from other members of the BEG group by the unusual um-
brella-like fl ange formed by proliferation of the tissues of
the micropyle ( Berridge, 1911 ; Martens, 1971 ). The devel-
opment of such a structure may only be possible given the
protection afforded by the outer seed envelope. In all the
seeds described here, the tip of the micropyle is missing, but
there is no indication of such a fl ange in any of the fossil
seeds.
The seed of Lignierispermum shares several characters with
seeds of Gnetum . Both have cellular closure of the micropyle,
and both have a seed envelope with an inner fi brous layer, fol-
lowed by a layer of radiating sclerenchyma cells and an outer-
most layer of thin-walled cells.
Buarcospermum, Lignierispermum, Lobospermum, Rugo-
nella, and seeds of Erdtmanithecales Erdtmanithecales are
an extinct group of seed plants established by Friis and Peder-
sen (1996) to accommodate fossil plants that produced the dis-
persed pollen grains of Eucommiidites Erdtman. Pollen of
Eucommiidites is characterized by a distinct distal colpus that is
anked by two lateral colpi or a subequatorial ring-colpus. The
pollen wall is tectate, sometimes fi nely perforate, and has a
Figs. 95 98. Schematic line drawings through micropylar area of Lignierispermum maroneae in longitudinal (95) and transverse sections (96 98). Yel-
low = integument; dark green = inner sclerenchyma layer of seed envelope, light green = outer sclerenchyma layer of seed envelope. Figs. 96 – 98 at succes-
sively lower levels indicated with arrows on Fig. 95 . Scale bar Fig. 95 = 1 mm; Figs. 96–98 (at Fig. 98) = 0.5 mm. Compare with Figs. 24 – 28, 128 – 131 .
275
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
nella in the lack of long fi brous, arched cells in the inner layer
of the seed envelope. Due to the lignitic preservation , X-ray
studies of Erdtmanispermum have so far failed to provide de-
tails of the micropylar closure.
Buarcospermum, Lignierispermum, Lobospermum, Rugo-
nella, and seeds of Bennettitales Bennettitales are an impor-
tant but entirely extinct group of Mesozoic plants that are
diverse and widespread from the mid-Triassic through the Ju-
rassic and into the Late Cretaceous. Bennettitales are known
mostly from their pinnate, cycad-like leaves, but there are also
diverse fl ower-like reproductive structures preserved as impres-
sions, compressions, or permineralizations. Seeds are typically
small and borne in dense aggregations interspersed with in-
terseminal scales on a domed or conical receptacle (e.g., Lignier,
1894 ; Wieland, 1906 ; Harris, 1969 ). In some Bennettitales, the
reproductive structures are bisexual with microsporangiate or-
gans surrounding the ovulate structures. Other reproductive
structures are unisexual with microsporangiate organs and
seeds borne separately ( Harris, 1969 ; Watson and Sincock,
1992 ). Ovulate reproductive structures are often surrounded by
large tepal-like structures that result in a variety of different
“ fl oral morphologies ( Watson and Sincock, 1992 ). The struc-
ture of the pollen-producing organs is less clear, but they often
appear fused to the tepal-like structures to form a shallow cup
( Harris, 1969 ; Watson and Sincock, 1992 ).
The organization of the seeds in Bennettitales has been a
matter of much discussion. Seeds preserved as compressions
such as Vardekloeftia sulcata Harris from the Late Triassic of
Greenland ( Harris, 1932 ; Pedersen et al., 1989a ) often show
well-preserved cuticles from the various tissues. In Vardek-
loeftia Harris, there is an inner indistinct layer that is partly
fused to and surrounded by another, well-cutinized layer that
is extended apically into a long tube. This tube contains mono-
colpate pollen grains. The tube projects beyond an additional
outer seed layer in a similar way to the micropylar tube of
Gnetales, Erdtmanithecales, and the fossil seeds described
here. The additional outer layer consists of sclerenchymatous
tissue covered by an outer cuticle. The corresponding inner
cuticle of this outer layer is free from the cuticle of the integu-
ment except at the base. The nature of the various cuticles and
the remains of the tissues that they enclose in Vardekloeftia
strongly suggest that the innermost, thin layer is nucellus, the
layer that forms the tube is integument, and the additional
outer sclerenchymatous layer is equivalent to the seed enve-
lope of Gnetales, Erdtmanithecales, and the fossil seeds de-
scribed here. The elongated tube containing pollen grains is
therefore the micropylar tube rather than a nucellar plug as
suggested by Rothwell and Stockey (2002) . It is interesting
that this structure is so clearly seen in Vardekloeftia, which is
one of the earliest Bennettitales and is distinguished from Ju-
rassic and Cretaceous taxa by the much smaller number of
seeds per ovulate head (about 20 in contrast to hundreds in
younger taxa).
Further support for the interpretation that the ovules of
Bennettitales share a common ground plan with seeds of
Buarcospermum , Lignierispermum , Lobospermum, Raun-
sgaardispermum, Rugonella , Gnetales, and Erdtmanithecales
comes from other bennettitalean ovulate structures preserved
as compressions (e.g., Bennettites crossospermus Harris, Wil-
liamsonia himas Harris) and permineralizations ( Friis et al.,
2007 ). In Bennettites crossospermus Harris (1932, g. 14H, pl.
11), described and illustrated a micropylar plate through
Table 1. Comparison of seeds from the Early Cretaceous of Portugal and eastern North America described in this paper.
Species Locality Size (L × W) (mm) Envelope shape in
cross section Outer surface of
envelope Outer sclerenchyma cells of
seed envelope Radially extended cells in
outer layer of seed envelope Fiber arches in inner
layer of envelope
Buarcospermum
tetragonium
Buarcos, Torres-Vedras,
Catefi ca, Puddledock
1.8 – 2.2 × 1.4 – 1.5 4-angled, radially
symmetrical
Smooth Isodiametric, irregular shape Present Many short,
closely spaced
Lobospermum
stampanonii
Puddledock 3.8 × 1.7 4-angled, radially
symmetrical
Smooth to slightly
rugulate
Longitudinally elongate, equiaxial
in TS
Absent Few broad
Lobospermum glabrum Famalic ã o, Catefi ca 2.3 – 4.8 × 1.5 – 2 4-angled, radially
symmetrical
Smooth to slightly
rugulate
Longitudinally elongate, cells
toward inside taller in TS
Absent Few broad
Lobospermum rugosum Puddledock, Catefi ca 3.7 – 4.1 × 1.15 – 1.6 4-angled, radially
symmetrical
Rugulate Longitudinally elongate, cells
toward outside taller in TS
Absent Few broad
Rugonella
trigonospermum
Puddledock 2.5 × 2.3 3-angled, bilaterally
symmetrical
Rugulate Longitudinally elongate, cells
toward outside taller in TS
Absent Few broad
Lignierispermum
maroneae
Puddledock, Catefi ca 2.7 – > 3.1 × 1.3 – 1.7 4-angled,
bisymmetrical
Smooth Longitudinally elongate, equiaxial
in TS
Present Fibers not
arched
Note: TS = transverse section
276 American Journal of Botany [Vol. 96
277
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Figs. 99 121. Reconstructions of selected isolated seeds from the Early Cretaceous of Denmark, Portugal and eastern North America. All have the
same ground plan with a thin membranous integument extended into a long micropylar tube and surrounded by a partly sclerenchymatous two-, three- or
four-angled seed envelope: note variation in size, shape, and surface ornamentation. Schematic line drawings. 99, 100. Lateral and apical view of Raun-
sgaardispermum lusitanicum , Juncal locality, Portugal. 101, 102. Lateral and apical view of Erdtmanispermum balticum , C. Nielsen locality, Bornholm,
Denmark. 103, 104. Lateral and apical view of Buarcospermum tetragonium , Buarcos locality, Portugal. 105, 106. Lateral and apical view of Ephedra
drewriensis , Drewry s Bluff locality, Virginia, USA 107, 108. Lateral and apical view of Ephedrispermum lusitanicum , Torres Vedras locality, Portugal.
109, 110. Lateral and apical view of square seeds, Torres Vedras locality, Portugal. 111 113. Lateral and apical view of undescribed triangular seed,
Puddledock locality, Virginia, USA 114, 115 . Lateral and apical view of Lignierispermum maroneae , Puddledock locality, Virginia, USA 116, 117. Lateral
and apical view of Rugonella trigonospermum , Puddledock locality, Virginia, USA 118, 119. Lateral and apical view of Lobospermum stampanonii , Pud-
dledock locality, Virginia, USA 120, 121. Lateral and apical view of Lobospermum glabrum , Famalic ã o locality, Portugal. See text for references.
which the micropylar tube projects. We think that this micro-
pylar plate probably corresponds to the envelope seen in Cy-
cadeoidea morierei as well as the seeds described here. A similar
situation is illustrated in a specimen of Williamsonia himas from
the Middle Jurassic of Yorkshire, UK ( Harris, 1969 , fi g. 60K).
The permineralized reproductive structures of Bennettitales,
that are usually described as species of Cycadeoidea Buckland
or Williamsonia Carruthers, are in many respects more infor-
mative than the compressions fossils. However, because of the
dense packing of the various organs in the ovulate structures,
organizational details for the various tissues are not always
straightforward to interpret.
Among the permineralized fossils is a well-preserved bennet-
titalean ovulate structure from Normandy variously referred to as
Williamsonia morierei Saporta et Marion, Bennettites morierei
(Saporta et Marion) Lignier, or Cycadeoidea morierei . The fossil
was discovered at the Vaches-Noires coastal exposures near Vil-
liers-sur-Mer and was described in detail by Lignier (1894) . The
exposure at Vaches-Noires consists mainly of Jurassic sedi-
ments, but above there are soft Early Cretaceous sediments of
Albian age. According to Rioult (1966; personal communication ,
2008), the fossil corresponds in preservation to other fossils
washed out of the Early Cretaceous sediments. In general, the
morphology and organization the specimen corresponds closely
to other Early Cretaceous ovulate structures assigned to Cy-
cadeoidea, such as C. albiana (Stopes) Wieland ( Stopes, 1918 )
and C. gibsoniana (Carruthers) Seward ( Solms-Laubach, 1891 ).
Here we refer to the Normandy specimen as C. morierei .
Cycadeoidea morierei is a small ovulate cone ~55 mm long
and 35 mm in diameter ( Lignier, 1894 ). Numerous small ovules
and interseminal scales are densely arranged on a conical recep-
tacle. The ovules are borne on long stalks and are surrounded
by interseminal scales that are fl attened proximally, but ex-
panded distally. The seeds are ~6 7 mm long and 2.5 3 mm in
diameter, elongate elliptical in lateral view ( Figs. 132 134,
136, 137 ) and four- to fi ve-angled in cross section ( Figs. 130,
131, 134 ). The ovulate structure has been sectioned, and some
of the sections as well as Lignier s original illustrations are still
available for study. In addition, several fragments of the cone
that were left after sectioning can still be examined. Among
these fragments are isolated seeds and interseminal scales,
which permit their morphology and structure to be examined
separately. Both seeds and interseminal scales appear to sepa-
rate easily indicating that they were discreet units in the repro-
ductive structure. This is also supported by the presence of
well-preserved cutinized epidermis with stomata on both organ
types ( Fig. 138 ). The separation may also be facilitated by the
relatively weak mineralization of Cycadeoidea morierei. In
other permineralized bennettitalean reproductive structures, the
precise limits of seeds and interseminal scales are sometimes
diffi cult to determine.
The seeds of C. morierei consist of a distinct outer sclerenchy-
matous tissue with several different zones. This outer sclerenchy-
matous tissue surrounds a thin inner tissue, which is extended
into a long, narrow tube ( Figs. 129, 135 ). Sections show that this
tube is hollow distally similar to the micropylar tube seen in Gn-
etales and other seeds of the BEG group. In the middle and proxi-
mally, the micropylar tube is closed by several layers of small
equiaxial cells. At the base of the micropyle, the central part
shows an irregularly defi ned cavity that is very similar to the cen-
tral, apparently lysigenous cavity of Gnetum ( Berridge, 1911 ).
The most straightforward interpretation is that the thin inner layer
that forms the tube is the integument. In this case, the mechanism
of closure is similar to that in Gnetum, as originally pointed out
by Berridge (1911) , but without the umbrella-like closing struc-
ture. Internal to the integument and adhering closely to it is an-
other tissue that we interpret as the nucellus.
The outer sclerenchymatous envelope of Cycadeoidea mori-
erei enclosing the integument has three different layers. The
inner layer is thin over most of the seed and consists of elon-
gated and longitudinally aligned fi bers (couche fi breuse of
Lignier, 1894 ). Subapically, this fi brous layer is thicker and ex-
tended radially toward the corners of the seeds to form four or
ve wing-like crests that project through the middle zone of the
seed envelope in a star-shaped pattern ( Figs. 130, 131, 34 ). The
wing-like crests become less prominent below the micropylar
region and disappear at about the middle of the seed ( Figs. 132
134, 136, 137 ). The middle layer consists of thin-walled and
almost equiaxial and thin-walled cells (tissu charnu of Lignier,
1894 ). Over most of the seed, this middle zone of C. morierei is
one to two cell layers thick, but it thickens toward the micropy-
lar region and fi lls out the space between the wing-like crests
( Figs. 129 131, 135, 136 ). Subapically, the seed envelope of C.
morierei has an outer layer of strongly enlarged and radially
extended cells (l assise pliss é e, ou rayonnante of Lignier, 1894 )
( Figs. 129 131, 135 ). The outer epidermis of the seed envelope
is well developed ( Figs. 135, 137, 138 ) with distinct paracytic
stomata ( Fig. 138 ).
We interpret the outer envelope with its three layers as cor-
responding to the seed envelope of Ephedra, the inner seed en-
velope of Gnetum, and the seed envelope of Buarcospermum ,
Ephedrispermum , Erdtmanispermum , Lignierispermum , Lo-
bospermum , Raunsgaardispermum , and Rugonella . It is partic-
ularly similar to the inner seed envelope of Gnetum. Both have
subapically enlarged and radiating sclerenchyma cells. This
similarity was also pointed out by Berridge (1911) . A similar
subapical zone of strongly extended radiating cells is also found
in Lignierispermum ( Figs. 82, 83, 87 ).
Based on the similarities between Cycadeoidea morierei and
seed architecture of extant and fossil Gnetales, Erdtmanithe-
cales, and the four genera of dispersed seeds described in this
paper, we think it very likely that when suitably preserved, and
278 American Journal of Botany [Vol. 96
cospermum and Lignierispermum clearly show a thin integu-
ment, which is largely fused to the nucellus and that extends
apically into a long, slender micropylar tube (e.g., Figs. 10, 15,
82, 83 ). At the tip, the tube is open, but below it is solid: the
micropylar canal having been closed by growth of the surround-
ing cells of the integument that comprise the micropylar tube. A
similar structure occurs in Cycadeoidea morierei (see above)
and also appears to be present in other bennettitalean seeds (see
below). Below the level of the micropylar canal in at least some
specimens ( Fig. 83 ), there is evidence of a depression in the
nucellus that could be interpreted as a pollen chamber.
If the reinterpretation of bennettitalean seed architecture pre-
sented here is borne out by future research, then it will require
revision of most current interpretations of seeds attributed to
genera such as Cycadeoidea and Williamsonia . For example, in
C. albianus (Stopes) Wieland tissues referred to as (1) the in-
ner thin-walled cells; (2) the fi brous layer; (3) the stone layer;
Figs. 122 127. Selection of square seeds from the Early Cretaceous of Portugal and eastern North America. SEM images; scale bar for all, shown
in Fig. 122 , = 1 mm. Figs. 122, 123 . S154562, sample Torres Vedras 43. Figs. 124, 126 . PP53366, sample Puddledock 082. Fig. 125 . S154564, sample
Torres Vedras 43. Fig. 127 . PP53364, sample Puddledock 082. 122, 123. Lateral and apical view of seed, Torres Vedras locality, Portugal: note long apical
projection and central pointed micropylar area. 124, 126. Lateral and apical view of seed, Puddledock locality, Virginia, USA: note long apical, straight
projections and central, pointed micropylar area. 125. Lateral view of seed without apical projections, Torres Vedras locality, Portugal. 127. Lateral view
of seed, Puddledock locality, Virginia, USA: note recurved apical projections and strongly rugulate surface.
when studied in suffi cient detail, the seeds of all previously de-
scribed Bennettitales will be shown to have a nucellus sur-
rounded by two coverings: an integument, fused to a greater or
less extent to the nucellus, and an outer seed envelope. This
interpretation, which has been raised in the past (e.g., Solms-
Laubach, 1891 ; Berridge, 1911 ), was rejected in the early 20th
century (e.g., Lignier, 1911 ; Stopes, 1918 ). Since then, it has
rarely been discussed. We believe that the similarities between
the seeds described here and those of Cycadeoidea morierei
warrant its revival.
In addition to similarities in the anatomy of the seed enve-
lopes discussed here, the similarity between the elongated mi-
cropylar tube of fossil seeds such as Buarcospermum and
Lignierispermum and the so-called nucellar plug described in
permineralized bennettitalean material (e.g., Stopes, 1918 ;
Rothwell and Stockey, 2002 ; Stockey and Rothwell, 2003) is
especially important. SRXTM and PCXTM images of Buar-
279
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Among the isolated seeds described here, those of Buar-
cospermum and Lignierispermum are particularly similar to
seeds of Cycadeoidea morierei and other Bennettitales, as well
as to seeds of extant Gnetum . In C. morierei , as well as in Buar-
cospermum and Lignierispermum , the inner, fi brous scleren-
chyma layer of the seed envelope expands in the apical part of
the seed to form four or fi ve narrow wing-like crests. The ridges
are particularly pronounced in the subapical micropylar region
and radiate toward the outside of the seed envelope in a star-
shaped manner (compare Figs. 12, 87, 130, 131 ). A further
character that unites Buarcospermum and Lignierispermum
with C. morierei is the cellular closure of the micropylar canal.
In this respect, they are also similar to seeds of Gnetum and
Welwitschia , that have a cellular micropylar closure mechanism
( Martens, 1971 ).
Phylogenetic and ecological implications The isolated
seeds of Buarcospermum , Lignierispermum , Lobospermum ,
and Rugonella correspond in all the major features of their
structure and organization to seeds of Bennettitales, Erdtmani-
thecales, and Gnetales (the BEG group). Together with the
square seeds, phylogenetic analyses placed them inside the
BEG group as sister to Gnetales in a polychotomy with Ben-
nettitales and Erdtmanithecales ( Friis et al., 2007 ). More de-
tailed phylogenetic analyses will require more information on
the parent plants of Buarcospermum , Lignierispermum , Lobos-
permum , Rugonella , and similar fossils. We have not observed
pollen in any of the isolated seeds described here, and there is
no information on how the seeds were borne on the plant. There
is also no information on other parts of the plants such as
bracts, leaves, or axes that could be used for a more detailed
evaluation of their relationship within the BEG group.
In modern Gnetales, pollen are sealed inside the integument
either by cellular micropylar closure or by secretion. The presence
Figs. 128 131. Schematic line drawings comparing seeds of Gnetales and Bennettitales. Fig. 128 . Gnetum gnemon L; line drawing adapted from g.
114 in Martens (1971) and g. 1 in Berridge (1911) . Figs. 129 – 131 . Cycadeoidea morierei ; line drawings adapted from g. 28 in Lignier (1894) and new
observations. Yellow = integument; dark green = inner sclerenchyma of seed envelope, light green = outer sclerenchyma of seed envelope. 128. Longitudi-
nal section (LS) of Gnetum gnemon showing nucellus, integument, and seed envelope with radiating cells in the subapical region and epidermis; outermost
seed envelope not shown. 129. LS of Cycadeoidea morierei showing nucellus, integument, and seed envelope with radiating cells in the subapical region.
130. Transverse section (TS) of seed near base of micropyle showing the different layers of the seed envelope: inner fi brous layer with wing-like crests,
middle layer of thin-walled cells, outer layer of radiating cells, and epidermis. 131 . TS of ovulate structure near the surface showing apical part of four- or
ve-angled seeds at various levels and tips of micropyles with open micropylar canal; adapted from g. 6 in Lignier (1894) . Compare with Buarcospermum
tetragonium ( Figs. 24 – 28) and Lignierispermum maroneae ( Figs. 95 – 98) .
which form the seed coat proper , and perhaps the (4) deli-
quescent layer, and (5) the tubular cells of the cupule ( Stopes,
1918, p. 413 ) would all be part of the seed envelope. The struc-
ture interpreted as a plug of nucellar tissue in the micropyle
( Stopes, 1918, p. 413 ) would be the micropyle, formed by the
integument and occluded by closure tissue. We therefore reject
the previous interpretation by one of us ( Crane, 1985 ) that the
enlarged tubular cells ( cupule of Stopes, 1918 ) derived from
the cells of the seed stalk correspond to the envelope ( cupule )
of Vardekloeftia .
Other permineralized Bennettitales have the same structure as
Cycadeoidea albianus and can be reinterpreted in the same way.
For example, C. gibsoniaus (Carruthers) Seward from the Early
Cretaceous of southern England ( Friis et al., 2007 ). Similarly, in C.
maccafferyi Rothwell et Stockey (2002) and Williamsonia bockii
Stockey et Rothwell (2003), tissues described as sarcotesta and
sclerotesta would be part of the seed envelope, while the structure
interpreted as a nucellar plug would be the micropyle formed by
the integument but occluded by the closure tissue. Given that such
a nucellar plug has been reported for most permineralized Ben-
nettitales ( Rothwell and Stockey, 2002 ), we think it very likely that
all Bennettitales have an elongate, slender micropylar tube sur-
rounded by a much more robust outer envelope. The micropylar
tube will usually appear solid in both longitudinal and transverse
section as a result of the closure tissue and will at some levels ap-
pear to be part of the seed envelope because it is tightly adpressed
to it as a result of its expansion further down. However, if the tip of
the micropyle is preserved, the micropylar tube should be open
(e.g., Stockey and Rothwell, 2003, g. 3B ).
The outer envelope, which surrounds both the nucellus and
integument, is conventionally interpreted as the single (only)
integument. By the interpretation presented here, this layer (re-
ferred to in this paper as envelope ) is in fact an additional
(second) covering around the nucellus.
280 American Journal of Botany [Vol. 96
Figs. 132 – 138. Cycadeoidea morierei from the Early Cretaceous (Albian) of Vaches-Noires near Villiers-sur-Mer, France; fragments from holotype.
Figs. 132 134 . Tomographic reconstructions of seed. Figs. 135 138 . SEM images. Scale bars: Figs. 132 134, 136, 137 = 2 mm; Fig. 135 = 1 mm; Fig. 138 =
0.5 mm. 132 134. Seed showing the inner, fi brous sclerenchyma layer with its four subapical crests. 135. Broken seed showing integument, part of micro-
pylar tube, and seed envelope consisting of layer of inner, fi brous cells, layer of thin-walled cells, and a subapical, outer layer of radially extended cells.
136, 137. Seed with part of seed envelope missing showing inner, fi brous layer, apical crests, and remains of radiating cells and epidermis of seed envelope.
138. Surface of outer epidermis showing elongate cells and scattered paracytic stomata.
281
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
of a similar micropylar closure in the fossil taxa described here
suggests that they had similar reproduction and that the appar-
ent absence of pollen inside the seeds is due to the currently
limited observations and material. Each of the new taxa de-
scribed here are represented only by a few specimens, none of
the seeds have been macerated, and the resolution of the X-ray
images may not be suffi cient to recognize in situ pollen. How-
ever, another explanation for the lack of pollen inside the seeds
could be that pollen germination took place outside the integu-
ment as known for some conifers (e.g., Owens et al., 1995 ) and
has been suggested for Bennettitales (Stockey and Rothwell,
2003).
Notwithstanding the need for additional information, the dis-
tinctive architecture of Buarcospermum , Lignierispermum , Lo-
bospermum , and Rugonella is of exceptional phylogenetic
interest because of the strong similarities with seeds of Bennet-
titales, Erdtmanithecales, and Gnetales. Buarcospermum and
Lignierispermum in particular share many features with both
extinct Cycadeoidea and Gnetum. Buarcospermum , Lobosper-
mum , and Rugonella have chevrons of fi bers similar to those
seen in the winged seeds of Welwitschia . Similarly, Rauns-
gaardispermum combines seed characters of Ephedra with pol-
len characters of Bennettitales.
Previous studies have already identifi ed isolated seeds that
can be assigned to Ephedra based on the papillate lining
around the micropylar tube and in situ polyplicate Ephedra -
type pollen ( Rydin et al., 2006a ). Isolated seeds of Erdtmani-
thecales have also been identifi ed based on distinctive
Eucommiidites type pollen inside the micropyles. Other fossil
remains of Gnetales and Erdtmanithecales document that
these lineages were well established and diverse in the Early
Cretaceous, although they were not a dominant element of the
Early Cretaceous vegetation ( Crane, 1996 ; Friis and Pedersen,
1996 ). In contrast, the Bennettitales have long been recog-
nized as a prominent part of certain Early Cretaceous ecosys-
tems and are known mainly from abundant leaf fossils ( Watson
and Sincock, 1992 ).
Isolated seeds that can be assigned to the Bennettitales have
only been identifi ed from the Late Triassic ( Vardekloeftia , Ped-
ersen et al., 1989a ). It has generally been assumed that the seeds
of Bennettitales were perhaps not shed individually from the
ovulate structures, and in his extensive studies of the Middle
Jurassic fl oras of Yorkshire in which Bennettitales are abun-
dant, Harris (1969) failed to identify any dispersed bennetti-
talean seeds. The cutinized epidermis and abundant stomata on
outer surface of the Cycadeoidea morierei seeds and the in-
terseminal scales may indicate that these organs could poten-
tially survive exposure and dispersal as discrete units. The
defi nitive recognition of dispersed bennettitalean seeds in
Mesozoic fl oras would greatly facilitate comparison with the
material described here.
Buarcospermum , Lignierispermum , Lobospermum , and
Rugonella co-occur with various angiosperm fossils, including
many angiosperm seeds that are comparable to seeds of the
BEG group in their small size, and in having two layers around
the nucellus. It is also interesting that the outer integument in
many, apparently bitegmic, Early Cretaceous angiosperm seeds
is sclerenchymatous ( Friis et al., 2000b ). The full phylogenetic
implications of these observations still need to be worked out,
but they are important points of similarity. They also raise again
the possibility that the structural similarities among angio-
sperms, Bennettitales, Gnetales, and related groups, perhaps
refl ect underlying biological similarities that resulted in similar
ecological preferences.
LITERATURE CITED
Berridge , E. M. 1911 . On some points of resemblance between Gnetalean
and Bennettitean seeds. New Phytologist 10 : 140 – 144 .
Brenner , G. J. 1963 . The spores and pollen of the Potomac Group of
Maryland. Maryland Department of Geology, Mines and Water
Resources Bulletin 27 : 1 – 215 .
Brenner , G. J. 1967 . The gymnospermous affi nity of Eucommiidites
Erdtman, 1948. Review of Palaeobotany and Palynology 5 : 123 – 127 .
Chase , M. W. , D. E. Soltis , R. G. Olmstead , D. Morgan, D. H. Les,
B. D. Mishler, M. R. Duvall et al . 1993 . Phylogenetics of seed
plants: An analysis of nucleotide sequences from the plastid gene
rbc L. Annals of the Missouri Botanical Garden 80 : 528 – 580 .
Crane , P. R. 1985 . Phylogenetic analysis of seed plants. Annals of the
Missouri Botanical Garden 72 : 716 – 793 .
Crane , P. R. 1996 . The fossil history of Gnetales. International Journal
of Plant Sciences 157 : S50 – S57 .
Crane , P. R. , P. Herendeen , and E. M. Friis . 2004 . Fossils and plant phy-
logeny. American Journal of Botany 91 : 1683 – 1699 .
Crane , P. R. , and S. Lidgard . 1989 . Angiosperm diversifi cation and
palaeolatitudinal gradients in Cretaceous fl oristic diversity. Science
246 : 675 – 678 .
Crane , P. R. , and G. R. Upchurch . 1987 . Drewria potomacensis gen. et
sp. nov., an early Cretaceous member of Gnetales from the Potomac
Group of Virginia. American Journal of Botany 74 : 1722 – 1736 .
Dilcher , D. L. , M. E. Bernardes-De-Oliveira , D. Pons , and T. A.
Lott . 2005 . Welwitschiaceae from the Lower Cretaceous of north-
eastern Brazil. American Journal of Botany 92 : 1294 – 1310 .
Dinis , J. L. 2001 . Defi nic ã o da Formac ã o da Figueira da Foz Aptiano a
Cenomaniano do sector central da margem oeste ib é rica /Defi nition
of the Figueira da Foz Formation Aptian to Cenomanian of the cen-
tral sector of the western Iberian margin). Comunica ç õ es Instituto
Geol ó gico e Mineiro 88 : 127 – 160 .
Dischinger , J. B. 1987 . Late Mesozoic and Cenozoic stratigraphic and
structural framework near Hopewell, Virginia. U.S. Geological
Survey Bulletin 1567: 1 – 48.
Donoghue , P. C. J. , S. Bengston , X.-P. Dong , N. J. Gostling , T. Huldtgren ,
J. A. Cunningham , C. Yin , Z. Yue , F. Peng , and M. Stampanoni .
2006 . Synchrotron X-ray tomographic microscopy of fossil embryos.
Nature 442 : 680 – 683 .
Doyle , J. A. 1969 . Cretaceous angiosperm pollen of the Atlantic
Coastal Plain and its evolutionary signifi cance. Journal of the Arnold
Arboretum 50 : 1 – 35 .
Doyle , J. A. 1992 . Revised palynological correlations of the lower
Potomac Group (USA) and the Cocobeach sequence of Gabon
(Barremian-Aptian). Cretaceous Research 13 : 337 – 349 .
Doyle , J. A. , and L. J. Hickey . 1976 . Pollen and leaves from the mid-
Cretaceous Potomac Group and their bearing on early angiosperm evo-
lution. In C. B. Beck [ed.], Origin and early evolution of angiosperms,
139 206. Columbia University Press, New York, New York, USA.
Doyle , J. A. , and E. I. Robbins . 1977 . Angiosperm pollen zonation of
the continental Cretaceous of the Atlantic Coastal Plain and its ap-
plication to deep wells in the Salisbury Embayment. Palynology 1 :
43 – 78 .
Duan , S. 1998 . The oldest angiosperm — A tricarpous female reproduc-
tive fossil from western Liaoning Province, NE China. Science in
China 41 : 14 – 20 .
Endress , P. K. 2001 . The
owers in extant basal angiosperms and infer-
ences on ancestral fl owers. International Journal of Plant Sciences
162 : 1111 – 1140 .
Eriksson , O. , E. M. Friis , K. R. Pedersen , and P. R. Crane . 2000 . Seed
size and dispersal systems of Early Cretaceous angiosperms from
Famalic ã o, Portugal. International Journal of Plant Sciences 161 :
319 – 329 .
Friedman , W. E. 2006 . Embryological evidence for developmental labil-
ity during early angiosperm evolution. Nature 441 : 337 – 340 .
282 American Journal of Botany [Vol. 96
Friedman, W. E. 2009 . The meaning of Darwin s abominable mystery.
American Journal of Botany 96: 5 – 21 .
Friis , E. M. , P. R. Crane , and K. R. Pedersen . 1997 . Anacostia , a new
basal angiosperm from the Early Cretaceous of North America and
Portugal with monocolpate/trichotomocolpate pollen. Grana 36 :
225 – 244 .
Friis , E. M. , P. R. Crane , K. R. Pedersen , S. Bengtson , P. C. J.
Donoghue , and M. Stampanoni . 2007 . Phase contrast enhanced
synchrotron-radiation X-ray analyses of Cretaceous seeds link
Gnetales to extinct Bennettitales. Nature 450 : 549 – 552 .
Friis , E. M. , H. Eklund , K. R. Pedersen , and P. R. Crane .
1994a . Virginianthus calycanthoides gen. et sp. nov. A caly-
canthaceous fl ower from the Potomac Group (Early Cretaceous) of
eastern North America. International Journal of Plant Sciences 155 :
772 – 785 .
Friis , E. M. , and K. R. Pedersen . 1996 . Eucommiitheca , a new pol-
len organ with Eucommiidites pollen from the Early Cretaceous of
Portugal. Grana 35 : 104 – 112 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 1994b . Angiosperm o-
ral structures from the Early Cretaceous of Portugal. Plant Systematics
and Evolution 8 ( Supplement ): 31 – 49 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 1995 . Appomattoxia an-
cistrophora gen. et sp. nov., a new Early Cretaceous plant with simi-
larities to Circaeaster and extant Magnoliidae. American Journal of
Botany 82 : 933 – 943 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 1999 . Early angiosperm
diversifi cation: The diversity of pollen associated with angiosperm re-
productive structures in Early Cretaceous fl oras from Portugal. Annals
of the Missouri Botanical Garden 86 : 259 – 296 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 2000a . Fossil oral
structures of a basal angiosperm with monocolpate, reticulate-acol-
umellate pollen from the Early Cretaceous of Portugal. Grana 3 9 :
226 – 245 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 2000b . Reproductive
structure and organization of basal angiosperms from the Early
Cretaceous (Barremian or Aptian) of western Portugal. International
Journal of Plant Sciences 161 ( 6 Supplement ): S169 – S182 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 2004 . Araceae from the
Early Cretaceous of Portugal: Evidence on the emergence of mono-
cotyledons. Proceedings of the National Academy of Sciences, USA
101 : 16565 – 16570 .
Friis , E. M. , K. R. Pedersen , and P. R. Crane . 2006 . Cretaceous an-
giosperm fl owers: Innovation and evolution in plant reproduction.
Palaeogeography, Palaeoclimatology, Palaeoecology 232 : 251 – 293 .
Harris , T. M. 1932 . The fossil ora of Scoresby Sound East Greenland.
Part 3: Caytoniales and Bennettitales. Meddelelser om Gr ø nland 85:
1 – 133.
Harris , T. M. 1969 . The Yorkshire Jurassic Flora. III. Bennettitales. The
British Museum of Natural History (Natural History), London, UK.
Heimhofer , U. , P. A. Hochuli , S. Burla , J. M. L. Dinis , and H. Weissert .
2005 . Timing of Early Cretaceous angiosperm diversifi cation and
possible links to major paleoenvironmental change. Geology 33 :
141 – 144 .
Hickey , L. J. , and J. A. Doyle . 1977 . Early Cretaceous fossil evidence for
angiosperm evolution. Botanical Review 43 : 3 – 104 .
Hilton , J. , and R. M. Bateman . 2006 . Pteridosperms are the backbone
of seed-plant phylogeny. Journal of the Torrey Botanical Society 133 :
119 – 168 .
Hughes , N. F. 1961 . Further interpretation of Eucommiidites Erdtman
1948. Palaeontology 4 : 292 – 299 .
Krassilov , V. 1982 . Early Cretaceous fl ora of Mongolia. Palaeontographica
B 181 : 1 – 43 .
Krassilov , V. A. 1986 . New oral structures from the Lower Cretaceous of
Lake Baikal area. Review of Palaeobotany and Palynology 47 : 9 – 16 .
Kva č ek , J. , and B. Pacltov á . 2001 . Bayeritheca hughesii gen. et sp.
nov., a new Eucommiidites -bearing pollen organ from the Cenomanian
of Bohemia. Cretaceous Research 22 : 695 – 704 .
Lignier , O. 1894 . Structure et affi
nit é s du Bennettites morierei Sap. &
Mar. (sp.). E. Lanier, Caen, France.
Lignier , O. 1911 . Le Bennettites Morierei (Sap. et Mar.) Lignier se re-
produisait probablement par parth é nog é n è se. Bulletin de la Soci é t é
Botanique de France 11 : 224 – 227 .
Martens , P. 1971 . Les gn é tophytes. Gebr ü der Borntraeger, Berlin,
Stuttgart.
Mendes , M. M. , E. M. Friis , and J. Pais . 2008b . Erdtmanispermum jun-
calense sp. nov., a new species of the extinct order Erdtmanithecales
from the Early Cretaceous (Berriasian) of Portugal. Review of
Palaeobotany and Palynology 149 : 50 – 56 .
Mendes , M. M. , J. Pais , and E. M. Friis . 2008a . Raunsgaardispermum
lusitanicum gen. et sp. nov., a new seed with in situ pollen from
the Early Cretaceous (probably Berriasian) of Portugal: Further sup-
port for the Bennettitales-Erdtmanithecales-Gnetales clade. Grana
47 : 211 – 219 .
Mohr , B. A. R. , M. E. C. Bernardes-de-Oliveira , and R. F. Loveridge .
2007 . The macrophyte ora of the Crato Formation. In D. M. Martill,
G. Bechly, and R. F. Loveridge [eds.], The Crato Fossil Beds of Brazil:
Window into an Ancient World, 537 565. Cambridge University
Press, Cambridge, UK.
Owens , J. N. , G. L. Catalano , S. J. Morris , and J. Aitken-Christie .
1995 . The reproductive biology of Kauri (Agathis australis). I.
Pollination and prefertilization development. International Journal of
Plant Sciences 156 : 257 – 269 .
Pais , J. , and Y. Reyre . 1981 . Probl è mes pos é s par la population sporo-
pollinique d un niveau à plantes de la s é rie de Buarcos (Portugal).
Sociedade Geol ó gica de Portugal Boletim 22 : 35 – 40 .
Pedersen , K. R. , P. R. Crane , and E. M. Friis . 1989a . Morphology and
phylogenetic signifi cance of Vardekloeftia Harris (Bennettitales).
Review of Palaeobotany and Palynology 60 : 7 – 24 .
Pedersen , K. R. , P. R. Crane , and E. M. Friis . 1989b . Pollen organs and
seeds with Eucommiidites pollen. Grana 28 : 279 – 294 .
Pott , C. , J. H. A. van Konijnenburg-van Cittert , H. Kerp , and M.
Krings . 2007 . Revision of the Pterophyllum species (Cycadophytina:
Bennettitales) in the Carnian (Late Triassic) fl ora from Lunz, Lower
Austria. Review of Palaeobotany and Palynology 147 : 3 – 27 .
Qiu , Y. L. 2005 . Phylogenetic analyses of basal angiosperms based on
nine plastid, mitochondrial, and nuclear genes. International Journal
of Plant Sciences 166 : 815 – 842 .
Qiu , Y.-L. , J. Lee , F. Bernasconi-Quadroni , D. E. Soltis , P. S. Soltis ,
M. Zanis , E. A. Zimmer , et al . 1999 . The earliest angiosperms:
Evidence from mitochondrial, plastid and nuclear genomes. Nature
402 : 404 – 407 .
Quisumbing , E. 1925 . Stony layer in seeds of gymnosperms. Botanical
Gazette (Chicago, Ill.) 79 : 121 – 195 .
Rey , J. 1972 . Recherches g é ologiques sur le Cr é tac é inf é rieur de
l ’ Estremadura (Portugal). Servi ç os Geol ó gicos de Portugal, Mem ó rias,
nova s é rie 3 21: 1 – 477.
Rey , J. 1993 . Les unit é s lithostratigraphiques du groupe de Torres Vedras
(Estremadura, Portugal). Comunica ç õ es Instituto Geol ó gico e Mineiro
79 : 75 – 85 .
Rey , J. , J. L. Dinis , P. Callapez , and P. P. Cunha . 2006 . Da rotura con-
tinental à margem passiva, Composi ç ã o e evolu ç ã o do Cret á cico de
Portugal. Minist é rio da Economia e da Inova ç ã o, Lisbon, Portugal.
Rioult , M. 1966 . Sur l ’ age Albien de Cycadeoidea micromyela Moriere
(Bennettitin é e). Bulletin de la Soci é t é Linn é enne de Normandie, Caen,
10 è s é rie 7: 9 – 17.
Rocha , R. , G. Manuppella , R. Mouteride , C. Ruget , and G. Zbyszewski .
1981 . Carta geol ó gica de Portugal na escala de 1/50000. Not í cia
explicativa da folha 19-C Figueira da Foz. Servi ç os Geol ó gicos de
Portugal, Lisbon, Portugal.
Rodin , R. J. , and R. N. Kapil . 1969 . Comparative anatomy of the seed
coats of Gnetum and their probable evolution. American Journal of
Botany 56 : 420 – 431 .
Rothwell , G. W. , and R. A. Stockey . 2002 . Anatomically preserved
Cycadeoidea (Cycadeoidaceae), with a reevaluation of systematic
characters for the seed cones of Bennettitales. American Journal of
Botany 89 : 1447 – 1458 .
283
January 2009] Friis et al. Early Cretaceous mesofossils related to the BEG group
Rydin , C. , B. Mohr , and E. M. Friis . 2003 . Cratonia cotyledon gen. et sp.
nov.: A unique Cretaceous seedling related to Welwitschia. Proceedings
of the Royal Society of London, B, Biology Letters 270 : 29 – 32 .
Rydin , C. , K. R. Pedersen , P. R. Crane , and E. M. Friis . 2006a . Former
diversity of Ephedra (Gnetales): Evidence from Early Cretaceous seeds
from Portugal and North America. Annals of Botany 98 : 123 – 140 .
Rydin , C. , S. Q. Wu , and E. M. Friis . 2006b . Liaoxia (Gnetales):
Ephedroids from the Early Cretaceous Yixian Formation in China.
Plant Systematics and Evolution 262 : 239 – 265 .
Solms-Laubach , H. 1891 . On the fructifi cation of Bennettites gibso-
nianus , Carr. Annals of Botany 5 : 419 – 454 .
Soltis , D. E. , P. S. Soltis , and M. J. Zanis . 2002 . Phylogeny of seed
plants based on evidence from eight genes. American Journal of
Botany 89 : 1670 – 1681 .
Srinivasan , V. 1992 . Two new species of the conifer Glenrosa from the
Lower Cretaceous of North America. Review of Palaeobotany and
Palynology 72 : 245 – 255 .
Srinivasan , V. 1995 . Conifers from the Puddledock locality (Potomac
Group, Early Cretaceous) of eastern North America. Review of
Palaeobotany and Palynology 89 : 257 – 286 .
Stockey , R. A. , and G. W. Rothwell . 2003 . Anatomically preserved
Williamsonia (Williamsoniaceae): Evidence for bennettitalean repro-
duction in the Late Cretaceous of western North America. International
Journal of Plant Sciences 164 : 251 – 262 .
Stopes , M. C. 1918 . New bennettitean cones from the British Cretaceous.
Philosophical Transactions of the Royal Society of London, B,
Biological Sciences 208 : 389 – 440 .
Sun , G. , S. Zheng , D. L. Dilcher , Y. Wang , and S. Mei . 2001 . Early
angiosperms and their associated plants from western Liaoning,
China. Shanghai Scientifi c and Technological Education Publishing
House, Shanghai, China.
Takaso , T. , and B. Bouman . 1986 . Ovule and seed ontogeny in Gnetum
gnemon L. Botanical Magazine of Tokyo 99 : 241 – 266 .
Teixeira , C. , G. Zbyszewski , C. Torre de Assun ç ã o , and G.
Manuppella . 1968 . Carta geol ó gica de Portugal na escala de
1/50000. Not í cia explicativa da folha 23-C Leiria. Servi ç os Geol ó gicos
de Portugal, Lisbon, Portugal.
Thoday , M. G. , and E. M. Berridge . 1912 . The anatomy and morphology
of the infl orescences and fl owers of Ephedra. Annals of Botany 26 :
953 – 985 .
von Balthazar , M. , K. R. Pedersen , P. R. Crane , and E. M. Friis .
2007 . Potomacanthus lobatus gen. et sp. nov., a new fl ower of
probable Lauraceae from the Early Cretaceous (Early to Middle
Albian) of eastern North America. American Journal of Botany 9 4 :
2041 – 2053 .
von Balthazar , M. , K. R. Pedersen , P. R. Crane , and E. M. Friis .
2008 . Carpestella lacunata gen. et sp. nov., a new basal angio-
sperm fl
ower from the Early Cretaceous (Early to Middle Albian)
of eastern North America. International Journal of Plant Sciences
169 : 890 – 898 .
Watson , J. , and C. A. Sincock . 1992 . Bennettitales of the English
Wealden. Palaeontographical Society, London, UK.
Wieland , G. R. 1906 . American fossil cycads, vol. I. Carnegie Institution
Washington Publication 34 : 1 – 295 .
Wu , S.-Q. 1999 . A preliminary study of the Jehol fl ora from western
Liaoning. Palaeoworld 11 : 7 – 37 (in Chinese with English summary) .
Yang , Y. 2007 . Asymmetrical development in biovulate cones resulting
in uniovulate cones in Ephedra rhytidosperma (Ephedraceae). Plant
Systematics and Evolution 264 : 175 – 182 .
Yang , Y. , B.-Y. Geng , D. L. Dilcher , Z.-D. Chen , and T. A. Lott .
2005 . Morphology and affi nities of an Early Cretaceous Ephedra
(Ephedraceae) from China. American Journal of Botany 9 2 :
231 – 241 .
Zbyszewski , G. , F. Moitinho d Almeida, and C. Torre de Assun ç ã o .
1955 . Carta geol ó gica de Portugal na escala de 1/50000. Not í cia
explicativa da folha 30-C Torres Vedras. Servi ç os Geol ó gicos de
Portugal, Lisbon, Portugal.
Zbyszewski , G. , and C. Torre de Assun ç ã o . 1965 . Carta geol ó gica
de Portugal na escala de 1/50000. Not í cia explicativa da folha 30-D
Alenquer. Servi ç os Geol ó gicos de Portugal, Lisbon, Portugal.
... The seed-bearing structures of Dayvaultia with their opposite and decussate arrangement of bracts, surrounding radially symmetrical seeds that lack a wing and that are arranged in opposite pairs, are more similar to the situation in extant Gnetales. Current hypotheses suggest that extant Gnetales are closely related to Bennettitales and Erdtmanithecales as part of the BEG (Bennettitales, Erdtmanithecales, Gnetales) group (Friis et al. 2007(Friis et al. , 2009(Friis et al. , 2011(Friis et al. , 2013a(Friis et al. , b, 2014(Friis et al. , 2019. Alternative preserved internal structure and the central cup-shaped receptacle on which the seeds are borne. ...
... Transverse sections around L, the midlevel and K, toward the cone apex and showing the outlines of four seeds around the mid-level and eight seeds higher up seemingly in two rows; note the four poorly defined lobes of several of the seeds. The BEG group is united by the shared possession of chlamydospermous seeds in which each seed develops from a unitegmic ovule but is tightly enclosed by an envelope, most likely formed from two or more enclosing protective bracts (Yang 2004;Rydin et al. 2006a, b;Friis et al. 2009Friis et al. , 2019. Within the BEG group the most relevant comparisons are with the seed-bearing structures of Gnetales, because Dayvaultia differs from Bennettitales in showing no evidence of interseminal scales among the ovules and it is not known how the seeds of Erdtmanithecales are borne. ...
... Acanthocatia, Arazedispermum, Buarcospermum, Cattomia, Lignierispermum, Lobospermum, Quadrispermum, Rothwellia, Thodaya, Tomcatia). Among these, Lobospermum (Friis et al. 2009(Friis et al. , 2013a closely resembles Dayvaultia in possessing narrowly ovoid radially symmetrical seeds that are distinctively four-lobed in cross section with a prominently pointed micropylar region. ...
Article
A new kind of seed-bearing structure is described based on three-dimensional casts and partially permineralized small cones from the Upper Jurassic Brushy Basin Member of the Morrison Formation, in the Henry Mountains of Utah. Cones of Dayvaultia tetragona gen. et sp. nov. are obovate in lateral view, 10.0–11.0 mm long, square in cross-section and 5.1–8.0 mm wide, with a thick wall composed of four tightly adhering bracts that open apically to expose the tips of six or eight elongate, four-lobed seeds. Micro-CT scanning reveals that the seeds are borne on a cup-shaped receptacle in a regular opposite and decussate manner. This regular arrangement, as well as similarities of the seeds to several kinds of Early Cretaceous chlamydospermous seeds, including those of Lobospermum and Battenispermum, suggests a relationship to extant and Cretaceous members of Gnetales. The sedimentary context in which the cones occur, combined with their local abundance, suggests that Dayvaultia was common on intermittently inundated well-drained floodplains during Morrison times, enhancing insight into the vegetation that supported the diverse vertebrate faunas for which the Morrison Formation is well known. http://zoobank.org/urn:lsid:zoobank.org:pub:0ECD4B37-E6B6-4050-B45A-28D713321EB8
... Fossil plant remains were extracted from rock samples by sieving in water, using a hand-shower through a 125 μm net mesh. The adhering mineral matrix was removed by treatment with hydrofluoric (40% HF) and hydrochloric (10% HCl) acids, then thoroughly rinsed in water, following standard methods (Friis et al., 1988(Friis et al., , 2009. ...
Article
Shoots of cheirolepidiaceous conifers assigned to the fossil genus Frenelopsis are very common in Portuguese Early Cretaceous mesofossil floras. In this study, a new cheirolepidiaceous conifer Frenelopsis antunesii is described from the Lower Cretaceous (upper Aptian –lower Albian) of Figueira da Foz Formation at the Carregueira site, close to the small village of Juncal, in western-central mainland Portugal. The new fossil conifer is described based on morphological characters of vegetative shoots and cuticular features. The new species, Frenelopsis antunesii, is characterised by branching segmented shoots with three leaves per node, leaf surfaces distinctly covered by trichomes, leaves with thick cuticles and stomata arranged in short rows. The stomatal apparatus is composed of four or rarely five subsidiary cells. The morphological and anatomical features documented here support the view that Frenelopsis antunesii likely grew in a semiarid to arid climate.
... Their seeds are organized in the same way as BENNETTITALES Engler and EPHEDRACEAE Dumortier, and may reflect similar ecological preferences. The in situ fossils are normally from sedimentary sequences where ephedroid seeds are also common (Friis et al., 2009;Mendes et al., 2010). This indicates that their living environment was maybe similar to that of the plants of the EPHEDRACEAE Dumortier. ...
Thesis
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The eco-group classification based on the growth-form of plants (Eco-Plant model) is widely used for extant, Cenozoic, Mesozoic, and Paleozoic palaeoenvironmental reconstructions. However, for most Mesozoic dispersed sporomorphs, the application of the Eco-Plant model is limited, because either their assignment to a specific eco-group remains uncertain or the botanical affinities to plant taxa are unclear. A new database Sporopollen (http://www.sporopollen.com) focused mainly on Mesozoic sporomorphs is created. Currently, it has collected 100,610 sporomorph pictures, 59, 498 plant pictures, 31, 922 sporomorph descriptions. At the same time, from 63, 035 references, it has collected 2, 215, 162 occurrences for both sporomorph and non-sporomorph fossils. The collected plant data include 32, 972 genera from 946 families. The collected sporomorph pictures include 5, 857 genera. With the help of the database, 861 dispersed Mesozoic sporomorph genera of Bryophytes, Pteridophytes, and Gymnosperms are reviewed by comparing the unique outline and structure/sculpture of the sporomorph wall with that of modern plants and in situ fossil plants. The results show that 474 of them can be linked to their closest parent plants and Eco-Plant model at family or order level, but 387 of them can not because of the lack of detailed ultrastructure descriptions. The use of a light microscope (LM) for determination is one of the main reasons that some dispersed sporomorphs cannot be linked precisely to their parent plants. The presented eco-groups for disperse Mesozoic sporomorphs provide the possibility to identify detailed vegetation and palaeoenvironmental change in the Mesozoic, especially in the context of climate change. A new interface (http://www.sporopollen.com/sporemesozoicsegs.php?opencode=paper1) was created based on the reviewed result to quickly link the dispersed sporomorphs to past vegetation patterns and climatic changes. Users can upload their data to the database and in return get quick results. It can automatically link all of the Mesozoic and Cenozoic sporomorphs to their possible parent plants at phylum, order, or family level. It can also automatically link all of the Triassic and Jurassic sporomorphs to the Eco-Plant model to assess the effect of humidity (EPH) and the effect of temperature (EPT). By using 30 sporomorph samples from a 10 m thick lignite bed from the Upper Triassic Haojiagou Formation (Rhaetian) as an example, the palaeovegetation and palaeoenvironment of a peat-forming wetland near the Triassic-Jurassic boundary are discussed with the help of the Eco-Plant model. The results show that the palynoflora contains both Eurasian and Gondwanan elements, and is dominated by the spores and pollen of Bennettitales, Corystospermales, Ginkgoales, and Gleicheniales. At the Triassic/Jurassic boundary (Hettangian), the palynoflora significantly changes as Cyatheales spores become the dominant elements. We analyse assemblages in terms of an Eco-Plant model, which assigns the parent plants of the palynomorphs into five groups based on humidity and four groups based on temperature, and uses multivariate statistical analyses to infer palaeoclimate and palaeoenvironmental conditions. Results suggest that the palaeoclimate of the Rhaetian was generally wet and subtropical with short seasonal drought periods. Our analysis shows that an Eco-Plant model may be a useful tool to reveal past vegetation patterns and climate changes, applicable to other Mesozoic assemblages.
... Although the suggestions in Erdtman (1948) had proved unacceptable to subsequent workers, he may draw solace from its continued citation (e.g. Coiro et al., 2019) and the fact that it has given rise to the assignation of a new order -Erdtmanithecales (Pedersen et al., 1989;Friis et al., 2009). "Pollen et Spores", Vol. ...
Article
This paper examines the annotations within a copy of the first edition of the ‘bible’ of palynology – Text-book of Modern Pollen Analysis – by the Norwegian botanist Knut Fægri and his co-author, the Danish botanist Johannes Iversen, published in 1950. The marginalia are the work of Swedish geobotanist Gunnar Erdtman, made in his personal library copy of 'Fægri & Iversen'. All three palynologists were amongst the most prominent figures in the history of the field. Erdtman himself had earlier (1943) produced An Introduction to Pollen Analysis and very much saw himself as the master of the discipline. He was probably unaware that his comments would be open to scrutiny and this paper seeks to assess his observations of two would-be usurpers of his palynological crown. Apart from extensive notes, underlinings, drawings, and textual marks, he queried or contradicted factual statements and, pedantically, English usage and reference order. His use of such interaction is to be found elsewhere within his archives, although not to the same extent as seen in Fægri and Iversen’s classic tome. As well as an addition to the critical apparatus available for the appraisal of an academic’s work, the marginalia allow an insight into the thinking of a pioneer scientist, and they reveal a spontaneity and a persona which might otherwise be hidden.
... All samples were collected from the same dark grey clay horizon, rich in fossil plants fragments. It contains a large variety of angiosperm fruits, seeds and flowers (Friis et al., 1994(Friis et al., , 1999(Friis et al., , 2011, abundant fragments of cheirolepidiaceous and other conifers Mendes and Kvaček, 2020;Kvaček and Mendes, 2020), several non-angiosperm seed plants (Friis et al., 2009;, fragments of thalloid liverworts and megaspores ascribed to Selaginellaceae. A preliminary palynological study of the same samples has documented a palynoflora mainly characterized by fern spores, gymnosperm pollen (including pollen grains of Classopollis), and a few angiosperm pollen grains (Mendes, in progress). ...
Article
A new cheirolepidiaceous conifer Watsoniocladus cunhae sp. nov. J.Kvaček et M.M.Mendes is described from the Early Cretaceous of Catefica in the Lusitanian Basin, Estremadura region, western Portugal. The new species Watsoniocladus cunhae has been established based on sterile twigs showing decussately arranged s-shaped leaves equipped with stomata surrounded by papillae and arranged in short rows. The new species is compared to all already-published species assigned to Watsoniocladus. Additionally, based on the newly observed morphological features in the Portuguese material (cuticle characters), we transfer two species from Cupressinocladus (Cupressaceae) to Watsoniocladus (Cheirolepidiaceae): Watsoniocladus itieri (Saporta) comb. nov. from the late Kimmeridgian of southern Jura (France) and Watsoniocladus crassirameus (Zheng Y.Cao) comb. nov. from the Early Cretaceous of China.
... Their seeds are organized in the same way as BENNETTITALES Engler and EPHEDRACEAE Dumortier, and may reflect similar ecological preferences. The in situ fossils are normally from sedimentary sequences where ephedroid seeds are also common (Friis et al., 2009;Mendes et al., 2010). This indicates that their living environment was maybe similar to that of the plants of the EPHEDRACEAE Dumortier. ...
Article
Full-text available
The ecogroup classification based on the growth-form of plants (Eco-Plant model) is widely used for extant, Cenozoic, Mesozoic, and Paleozoic paleoenvironmental reconstructions. However, for most Mesozoic dispersed sporomorphs, the application of the Eco-Plant model is limited because either their assignment to a specific ecogroup remains uncertain or the botanical affinities to plant taxa are unclear. By comparing the unique outline and structure/sculpture of the wall of dispersed sporomorph to the sporomorph wall of modern plants and fossil plants, 861 dispersed Mesozoic sporomorph genera of Bryophytes, Pteridophytes, and Gymnosperms are reviewed. Finally, 474 of them can be linked to their closest parent plants and Eco-Plant model at family or order level. Based on the demands of the parent plants to different humidity conditions, the Eco-Plant model separates between hydrophytes, hygrophytes, mesophytes, xerophytes, and euryphytes. Additionally, due to different temperature demands a separation in megathermic, mesothermic, microthermic, and eurythermic plants is possible. In the Mesozoic, both spore-producing and pollen-producing plants are adapted to different kinds of humidity. The concept to use the spore/pollen ratio to reflect the hygrophytes/xerophytes ratio is therefore questionable. The presented ecogroups for dispersed Mesozoic sporomorphs now allow identifying at least relative plant, paleoenvironmental and paleoclimate changes in Mesozoic sedimentary records.
... The nucellus apex had a beak at the apex but probably lacked a pollen chamber, although contrasting interpretations exist (reviewed by Rothwell et al., 2009). The ovules had an unvascularized integument that was free from the nucellus above the chalaza; depending on interpretation, it enclosed either a vascularized nucellus (Rothwell et al., 2009) or a second integument that was fused to the nucellus for most of its length (Friis et al., 2007;Friis, Pedersen & Crane, 2009). ...
Article
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The ovule and its developmental successor, the seed, together represent a highly characteristic feature of seed plants that has strongly enhanced the reproductive and dispersal potential of this diverse group of taxa. Ovules encompass multiple tissues that perform various roles within a highly constrained space, requiring a complex cascade of genes that generate localized cell proliferation and programmed cell death during different developmental stages. Many heritable morphological differences among lineages reflect relative displacement of these tissues, but others, such as the second (outer) integuments of angiosperms and Gnetales, represent novel and apparently profound and independent innovations. Recent studies, mostly on model taxa, have considerably enhanced our understanding of gene expression in the ovule. However, understanding its evolutionary history requires a comparative and phylogenetic approach that is problematic when comparing extant angiosperms not only with phylogenetically distant extant gymnosperms but also with taxa known only from fossils. This paper reviews ovule characters across a phylogenetically broad range of seed plants in a dynamic developmental context. It discusses both well‐established and recent theories of ovule and seed evolution and highlights potential gaps in comparative data that will usefully enhance our understanding of evolutionary transitions and developmental mechanisms.
Article
A new taxon, Skyttegaardia galtieri, is described based on microsporangiophores with Monosulcites/Cycadopites pollen isolated from clays collected at the Skyttegård locality, island of Bornholm, Denmark, which are of earliest Cretaceous (Berriasian) age. Each microsporangiophore consists of a short, massive proximal fertile stalk-like portion with a truncate base, and a long sterile distal extension. A cavity on each side of the median line of the stalk-like portion, partially encloses a sporangium that dehisces by a longitudinal slit. The long distal extension tapers to a slender point and is curved toward the inferred adaxial side. The extension is irregularly angular in cross-section and the cuticle is thick with deep stomatal pits. The organization of the microsporangiophore, the in situ pollen and stomatal features suggest relationship with extant Cycadales. However, in all extant and fossil cycads there are usually many more sporangia per microsporangiophore, typically in groups of two to five, and they are borne on the surface of the proximal stalk-like portion rather than embedded in its tissues. These differences preclude secure inclusion of Skyttegaardia in Cycadales and open the possibility that these microsporangiophores were produced by a group of extinct plants, the other parts of which remain to be identified. The thick cuticle and sunken stomata of Skyttegaardia, together with the embedded sporangia, suggest adaptation to water stress, which is also consistent with the xeromorphic traits seen among the leaf fragments in the Skyttegaard flora and the arid conditions inferred from geological–geochemical proxies.
Article
Premise of research. The Puddledock mesofossil flora from Virginia is the richest source for studying structurally preserved plant fossils in the Early Cretaceous Potomac Group sequence. Together with other mesofossil floras from the Potomac Group and also from Portugal, it is key for direct assessment of the structure, relationships, and reproductive biology of early angiosperms. In this study, a new multiparted floral structure from the Puddledock locality is analyzed, and its phylogenetic relationships are discussed. Methodology. The fossil was extracted from unconsolidated clays and sands through sieving in water. Adhering sediment was removed using HF and HCl followed by rinsing in water. External and internal features were studied using scanning electron microscopy and synchrotron radiation X-ray tomographic microscopy. Phylogenetic analyses were carried out by adding the features of the fossil flower to an existing morphological data set for extant angiosperms. Pivotal results. A new taxon, Melloniflora virginiensis gen. et sp. nov., is established on the basis of a small multiparted floral structure that has several series of free stamens (ca. 50) and carpels (21) borne on a flattened receptacle. Stamens have a broad, short base, and dehiscence is introrse. Ovules are borne in two rows on either side of the ventral suture of the carpels. Abundant secretory cells occur in all tissues. Melloniflora is related to extant early-diverging members of the Magnoliales but also has features found among extant taxa of other early-diverging angiosperm lineages such as Austrobaileyales. Conclusions. Melloniflora adds to the knowledge of plants related to extinct magnoliids from the Early Cretaceous. It shows a combination of features not seen in any extant taxon. Melloniflora contributes to the evidence of considerable extinct diversity at an early stage in angiosperm evolution, especially among clades that today are represented by only a few relatively species-poor lineages.
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Introduction Plant fossils from the Crato Formation are not only remarkable because of their beauty, but equally because of their scientific value, being on the cusp of the gymnosperm decline and the angiosperm radiation. Many of these fossils are preserved more or less entire, often with roots, stems, leaves, sporangia and flowering structures attached; there is also palaeosoil present in some specimens (Figure 19.1). The more or less complete fossils are not only attractive, but are of immense importance to the palaeobotanist, who often has to deal with dispersed organs, of which the natural connection remains unknown, until a more complete specimen is found. The original organic material of the Crato plant fossils is generally covered or replaced by goethite, a hydrated iron oxide, which causes the rusty, conspicuous colouring of the weathered fossils. Often, they are very weathered, poorly preserved and can only be seen as reddish brown impressions on the light yellowish slabs. In rare cases, mainly in specimens coming from layers at the base of the section, black organic material with cellular structures can be preserved. Then, fine details, even of reproductive organs – the most indicative parts concerning the taxonomic evaluation of a plant – may be observed three-dimensionally with scanning electron microscopy (SEM). The palaeoflora is known to be relatively diverse, but has not been fully described. It is now being investigated by an international team of researchers from various Brazilian and European institutions (FAPESP/Fundaçao de Amparo à Pesquisa do Estado de São Paulo).
Article
A new genus and species of fossil angiosperm (Appomattoxia ancistrophora) is established based on well-preserved fruiting units and associated pollen from the Early Cretaceous (Early or Middle Albian) Puddledock locality in the Potomac Group sequence of Virginia, eastern North America. Fruiting units are small, unilocular, and with a single, pendulous, orthotropous seed. The fruit surface is characterized by densely spaced unicellular spines with hooklike tips, which probably functioned in biotic dispersal. Pollen grains adhering to the stigmatic area of many specimens are monocolpate and tectate with granular to columellate infratectal structure, and are similar to dispersed grains assigned to Tucanopollis and Transitoripollis. Comparison of fossil Appomattoxia ancistrophora with extant plants reveals an unusual combination of characters that includes similarities with some magnoliid taxa, particularly Piperales (Piperaceae, Saururaceae) and Laurales (Chloranthaceae), as well as the monotypic ranunculid family Circaeasteraceae. Appomattoxia ancistrophora differs from extant Piperales in having a pendulous rather than erect ovule, and differs from extant Circaeaster in details of the fruit wall, as well as the presence of monosulcate rather than tricolpate pollen.