Semiaquatic adaptations in a giant predatory dinosaur

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DOI: 10.1126/science.1258750
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Abstract
We describe adaptations for a semiaquatic lifestyle in the dinosaur Spinosaurus aegyptiacus. These adaptations include retraction of the fleshy nostrils to a position near the mid-region of the skull and an elongate neck and trunk that shift the center of body mass anterior to the knee joint. Unlike terrestrial theropods, the pelvic girdle is downsized, the hindlimbs are short, and all of the limb bones are solid without an open medullary cavity, for buoyancy control in water. The short, robust femur with hypertrophied flexor attachment and the low, flat-bottomed pedal claws are consistent with aquatic foot-propelled locomotion. Surface striations and bone microstructure suggest that the dorsal “sail” may have been enveloped in skin that functioned primarily for display on land and in water.
DOI: 10.1126/science.1258750
, 1613 (2014);345 Science et al.Nizar Ibrahim
Semiaquatic adaptations in a giant predatory dinosaur
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ACKNO WLEDGM ENTS
Data discussed in this paper can be found in the supplementary
materials. All artifacts are stored at the Institute of Archeology
and Ethnography, Yerevan, Armenia. We thank the following
organizations for their financial support: the University of
Connecticut [20082014: Norian Armenian Programs Committee,
College of Liberal Arts and Sciences (CLAS), Office of Global
Affairs, Study Abroad; and CLAS Book Committee]; the UK
Natural Environment Research Council (grant IP-1186-0510), the
L. S. B. Leakey Foundation (2010 and 2011), the Irish Research
Council (2008 and 2009), and the University of Winchester.
We also thank P. Avetisyan and B. Yeritsyan, Institute of Archeology
and Ethnography, Republic of Armenia, for their collaboration.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/345/6204/1609/suppl/DC1
Materials and Methods
Supplementary Text
Figs. S1 to S16
Tables S1 to S7
References (39192)
Databases S1 and S2
27 May 2014; accepted 19 August 2014
10.1126/science.1256484
PALEONTOLOGY
Semiaquatic adaptations in a giant
predatory dinosaur
Nizar Ibrahim,
1
*Paul C. Sereno,
1
Cristiano Dal Sasso,
2
Simone Maganuco,
2
Matteo Fabbri,
3
David M. Martill,
4
Samir Zouhri,
5
Nathan Myhrvold,
6
Dawid A. Iurino
7
We describe adaptations for a semiaquatic lifestyle in the dinosaur Spinosaurus
aegyptiacus. These adaptations include retraction of the fleshy nostrils to a position
near the mid-region of the skull and an elongate neck and trunk that shift the center of
body mass anterior to the knee joint. Unlike terrestrial theropods, the pelvic girdle is
downsized, the hindlimbs are short, and all of the limb bones are solid without an open
medullary cavity, for buoyancy control in water. The short, robust femur with hypertrophied
flexor attachment and the low, flat-bottomed pedal claws are consistent with aquatic
foot-propelled locomotion. Surface striations and bone microstructure suggest that
the dorsal sailmay have been enveloped in skin that functioned primarily for display
on land and in water.
Bones of the predatory dinosaur Spinosaurus
aegyptiacus first came to light over a cen-
tury ago from Upper Cretaceous rocks in
Egypt (13) but were destroyed in World
War II (4). More recently, isolated teeth
and bones (5) and the anterior half of an adult
skull (6) have been discovered in the Kem Kem
beds of eastern Morocco (Fig. 1A) and equiv-
alent horizons in Algeria, but are insufficiently
complete to estimate the size, proportions, and
functional adaptations of this species. Here
we report the discovery of a partial skeleton of
S. aegyptiacus fromthemiddleoftheKemKem
sequence(Fig.1B),whichisprobablyCenomanian
in age (~97 million years ago) (7).
The subadult skeleton, here designated the neo-
type of S. aegyptiacus (8), preserves portions of the
skull, axial column, pelvic girdle, and limbs. It was
discovered in fluvial sandstone that has yielded re-
mains of the sauropod Rebbachisaurus (9)andthree
other medium-to-large theropods (an abelisaurid,
Deltadromeus,andCarcharodontosaurus)(7,10).
We regard two additional Kem Kem theropods,
Sigilmassasaurus brevicollis and S. maroccanus
(11,12), to be referable to S. aegyptiacus (8).
The neotype skeleton and isolated bones refer-
able to S. aegyptiacus were scanned with com-
puted tomography, size-adjusted, and combined
with a digital recreation of the original Egyptian
fossils (Fig. 2A, red). Missing bones were extrap-
olated between known bones or estimated from
those of other spinosaurids (6,13,14). The digi-
tal model of the adult skeleton of Spinosaurus
(Fig. 2A), when printed and mounted, measures
over 15 m in length, longer than Tyrannosaurus
specimens (~12.5 m) (15).
A concentrated array of neurovascular foramina
open on the anterior end of the snout and ap-
pear similar to foramina in crocodilians that
house pressure receptors that detect water move-
ment (8,16)(Fig.2Bandfig.S6).Theenlarged,
procumbent, interlocking anterior teeth are well
adapted for snaring fish (5,6)(Fig.2Bandfig.S4).
The fossa for the fleshy nostril is small and, unlike
any other nonavian dinosaur, is retracted to a
posterior position to inhibit the intake of water
(Fig. 2C and figs. S4 and S6) (8).
Most cervical and dorsal centra are elongate
compared to the sacral centra, resulting in a pro-
portionately long neck and trunk (Figs. 2A and 3
and tables S1 and S2). The anteriormost dorsal
centra, however, are proportionately short, ex-
ceptionally broad, and concavoconvex (Fig. 2D).
These characteristic vertebrae, the affinity of which
has been controversial (7,11,12), are referred
here to S. aegyptiacus, based on their association
with spinosaurid skeletons in Niger (8)andEgypt
(2).Thehorizontalcervicodorsalhingecreated
by these broad centra would facilitate dorsoven-
tral excursion of the neck and skull in the pur-
suit of prey underwater.
Thedistaltwo-thirdsofthetailcomprisesver-
tebrae with relatively short centra, diminutive
zygapophyses, and anteroposteriorly compressed
neural spines (Fig. 2G). The affinity of these
caudal elements has been uncertain (17), but
comparisons with associated remains from Egypt
(2) and more proximal caudals in the neotype
(Fig. 2A) allow referral to Spinosaurus. Short
centra and reduced neural arch articulations
enhance lateral bending during tail propulsion
in bony fish (18).
The forelimb has hypertrophied deltopectoral
and olecranon processes for powerful flexion and
extension (Fig. 2A). Elongate manual phalanges
(Fig. 2H) and less recurved, manual unguals that
SCIENCE sciencemag.org 26 SEPTEMBER 2014 VOL 345 ISSUE 6204 1613
1
Department of Organismal Biology and Anatomy, University
of Chicago, Chicago, IL 60637, USA.
2
Museo di Storia
Naturale di Milano, Corso Venezia 55, 20121 Milan, Italy.
3
School of Earth Sciences, University of Bristol, Queens
Road, Bristol, BS8 1RJ, UK.
4
School of Earth and
Environmental Sciences, University of Portsmouth, Burnaby
Road, Portsmouth, PO1 3QL, UK.
5
Laboratoire de
Géosciences, Faculté des Sciences Aïn Chock, Université
Hassan II, Casablanca, Morocco.
6
Intellectual Ventures, 3150
139th Avenue Southeast, Bellevue, WA 98005, USA.
7
Dipartimento di Scienze della Terra, Sapienza Università di
Roma, Piazzale Aldo Moro 5, 00185 Rome, Italy.
*Corresponding author. E-mail: nibrahim@uchicago.edu
RESEARCH |REPORTS
areprobablyreferabletoSpinosaurus (11)and
were possibly used in gaffing and slicing aquatic
prey suggest that the manus is proportionately
longer than in earlier spinosaurids (13,14).
Thepelvicgirdleandhindlimbareconsiderably
reduced in Spinosaurus (Fig. 2A). The surface
area of the iliac blade is approximately one-half
that in most other theropods (table S1), and the
supraacetabular crest that supports the hindlimb
is low (Fig. 2F). Hindlimb length is just over 25%
of body length (table S1). In a plot of forelimb,
hindlimb, and body length (Fig. 3), Spinosaurus
and other large theropods maintain fairly similar
forelimb lengths. Relative hindlimb length, however,
is noticeably less in the spinosaurid Suchomimus
(25%) and especially in Spinosaurus (19%) than
in other large tetanuran theropods.
Unlike other mid- or large-sized dinosaurs, the
femur in Spinosaurus is substantially shorter
than the tibia (Fig. 2, I and J, and table S1). In
smaller-bodied bipedal dinosaurs, short femoral
proportions indicate increased stride length and
enhanced speed. In Spinosaurus this is clearly
not the case, given the short hindlimb. The femur
in Spinosaurus has an unusually robust attach-
ment for the caudofemoral musculature, which
is anchored along nearly one-third of the femoral
shaft (Fig. 2I), suggesting powerful posterior
flexionofthehindlimb.Thearticulationatthe
knee joint for vertical limb support, in contrast,
is reduced. The distal condyles of the femur are
narrow, and the cnemial crest of the tibia is only
moderatelyexpanded(Fig.2,IandJ).Together
these features recall the shortened condition of
the femur in early cetaceans (19,20) and in extant
semiaquatic mammals that use their hindlimbs
in foot-propelled paddling (21).
Pedal digit I is unusually robust and long in
Spinosaurus:UnlikeAllosaurus or Tyrannosaurus,
1614 26 SEPTEMBER 2014 VOL 345 ISSUE 6204 sciencemag.org SCIENCE
Fig. 1. Geographic location and stratigraphic
position of the neotype skeleton of S. aegyptiacus.
(A) Locality (X), situated 18 km northeast of Erfoud
in southeastern Morocco. (B) Stratigraphic position
at the base of the upper unit of the Kem Kem beds,
with correlative positions of associated remains
of contemporary dinosaurs. Abbreviations: c, clay;
CT, Cenomanian-Turonian limestone; p, pebbles; P,
Paleozoic; sd, sandstone; st, siltstone.
Fig. 2. Semiaquatic skeletal adaptations in S. aegyptiacus.(A) Skeletal reconstruction in swimming
pose showing known bones (red) based on size-adjusted, computed tomographic scans of the neotype
(FSAC-KK 11888), referred specimens, and drawings of original bones (1). (B) Rostral neurovascular
foramina in lateral view (MSNM V4047 and a digital restoration of the holotypic lower jaw). (C)Narial
fossa in lateral view (MSNM V4047). (D) Anterior dorsal vertebra (~D1) in lateral, anterior, and posterior
views (UCRC PV601). (E) Dorsal neural spine (D8) in left lateral view (FSAC-KK 11888). (F) Left ilium in
lateral view (FSAC-KK 11888). (G) Mid-caudal vertebra (~CA30, reversed) in anterior and left lateral
views (UCRC PV5). (H) Right manual II-1 phalanx in proximal, lateral, and dorsal views (FSAC-KK 11888).
(I) Left femur in lateral view (FSAC-KK 11888). (J) Right tibia (reversed) in lateral view (FSAC-KK 11888).
(K) Right pedal digit III ungual in dorsal, lateral, and proximal views (FSAC-KK 11888). Abbreviations: af,
articular facet; ag, attachment groove; at, anterior trochanter; C2, 10, cervical vertebra 2, 10; CA1, caudal
vertebra 1; cc, cnemial crest; ce, centrum; clp, collateral ligament pit; D13, dorsal vertebra 13; ded, dorsal
extensor depression; dip, dorsal intercondylar process; fl, flange; ft, fourth trochanter; ftu, flexor tubercle;
lco, lateral condyle; nf, narial fossa; ns, neural spine; nvfo, neurovascular foramina; poz, postzygapophysis;
prz, prezygapophysis; S1, 5, sacral vertebra 1, 5; sac, supraacetabular crest; tp, transverse process.
Institutional abbreviations: FSAC, Faculté des Sciences Aïn Chock, Casablanca; MSNM, Museo di
Storia Naturale di Milano; UCRC, University of Chicago Research Collection, Chicago. Scale bars, 10 cm
in(B)to(D),(G),(H),and(K);and20cmin(E),(F),(I),and(J).
RESEARCH |REPORTS
the first phalanx of digit I in Spinosaurus is
the longest nonungual phalanx in the pes (fig.
S1) and would have been in contact with the
substrate in a stationary pose. The pedal un-
guals are proportionally large, long, low, and
flat-bottomed (Fig. 2K and figs. S1 and S2),
features that differ markedly from the deeper
recurved unguals in other large theropods.
The unguals in Spinosaurus are reminiscent of
the flattened pedal unguals of shorebirds that
do not perch (22). In addition, the toes of some
shorebirds have fleshy lobes and interdigital
webbing that enhance foot-propelled propulsion.
The lengthened digit I and flattened pedal un-
guals in Spinosaurus suggestthatthefootmay
have been adapted to traversing soft substrates
or webbed for paddling.
Increasesinbonemassanddensityarecom-
mon skeletal modifications in terrestrial verte-
brates transitioning to a semiaquatic existence (23).
In Spinosaurus, this was achieved by enlarging
midline display structures, eliminating open med-
ullary cavities in the long bones, and increasing
bone density. In subadult Spinosaurus,thedorsal
neural spines are composed primarily of dense
bone with only a narrow central zone of cancel-
lous bone (Fig. 4D), and long bones have solid
shafts (Fig. 4, A and C) with no development of
the open medullary cavity that is present in other
theropods, including early spinosaurids (Fig. 4B).
Bone density within the long bones, in addition,
is 30 to 40% greater in Spinosaurus than in other
theropods (8).
We estimated a center-of-body mass for a
flesh rendering of Spinosaurus created over
the digital skeleton (8). Center-of-mass estimates
for several theropods have been expressed as
a percentage of femoral length measured an-
teriorly from the hip joint (24). The center of
massinabipedmustbelocatedoverthemid-
dle one-third of the pes to generate a plausible
mid-stance pose (25). In our flesh rendering of
Spinosaurus, the center of body mass is po-
sitioned in front of both the hip and knee joints
at a distance greater than femur length (fig. S3),
suggesting that forelimb support was required
during terrestrial locomotion. Spinosaurus ap-
pears to have been poorly adapted to bipedal
terrestrial locomotion. The forward position of
the center of mass within the ribcage may have
enhanced balance during foot-propelled locomo-
tion in water.
These adaptations suggest that Spinosaurus
was primarily a piscivore, subsisting on sharks,
sawfish, coelacanths, lungfish, and actinopterygian s
that were common in the Kem Kem river system
(5,7,11). A long narrow skull and powerful fore-
limbs are also present in earlier spinosaurids, which
like Spinosaurus (26) have been interpreted as
predominantly piscivorous (13,14,27,28).
The locomotor adaptations outlined above,
however, mark a profound departure in form and
function from early spinosaurids. Prominent
among these are the reduced pelvic girdle; short
hindlimb; short femur; and long, low, flat-bottomed
pedal unguals, all of which can be verified in
the second partial skeleton described by Stromer
as Spinosaurus B(2,8). We note here that Spino-
saurus must have been an obligate quadruped
on land, the first discovered among theropod
dinosaurs, given the usual horizontal sacroiliac
joint and the anterior location of the estimated
center of body mass (8). Baryonyx was interpreted
as a facultative quadruped, based on its long skull
and neck and robust humerus (27), but this was
not confirmed by the discovery of more complete
hindlimb remains of the related Suchomimus (13).
In Spinosaurus we infer foot-powered paddling
from the relatively short femur with hypertro-
phied flexor attachment and strong pedal digit
I, as occurs in semiaquatic mammals such as early
cetaceans (1921). Low, flat-bottomed pedal unguals
are coincident with digital lobes or webbing in
SCIENCE sciencemag.org 26 SEPTEMBER 2014 VOL 345 ISSUE 6204 1615
Fig. 3. Ternary morphospace plot comparing
forelimb, hindlimb, and body length. Fore li mb
(humerus + radius + metacarpal II), hindlimb (femur +
tibia + metatarsal III), and body length (from snout
tip to posterior extremity of pelvic girdle) are plotted
as percentages of the sum of forelimb, hindlimb,
and body lengths in S. aegyptiacus and other large
tetanuran theropods (data from Table 1). Blue zone
shows the range of forelimb length, from 7% (Tyran-
nosaurus) to 12% (Allosaurus). Hindlimb length
(red zone) ranges from 34% (Allosaurus)to19%
(Spinosaurus). Abbreviations: Ac, Acrocanthosaurus;
Al, Allosaurus;Sp,Spinosaurus;Su,Suchomimus;Ty,
Tyrannosaurus.
hind limb
forelimb
body
Ty
Ac
Al
10
60
20
Sp
Su
70
80
40
30
Fig. 4. Bone microstructure and dorsal spine form. (A) Mid-shaft thin section of the right femur of
S. aegyptiacus (FSAC-KK 11888). (B) Mid-shaft thin section of the right femur of Suchomimus tenerensis
(MNN GAD608). (C) Cross-sectional view of right manual II-1 phalanx of S. aegyptiacus (FSAC-KK 11888).
(D) Thin section of a dorsal neural spine (distal section) in S. aegyptiacus (FSAC-KK 11888). (E)Dorsal
vertebrae with tall neural spines and spinal tendons in a cleared and stained specimen of Trioceros
(Chamaeleo)cristatus (FMNH 19886). Abbreviations: cb, cancellous bone; ec, erosional cavities; Hb,
Haversian bone; mc, medullary cavity; ns, neural spine; pb, primary bone; sc, scapula; st, striae; te,
tendon of multisegment spinal muscle. Institutional abbreviations: FMNH, Field Museum of Natural
History. Scale bars, 2 cm in (A) and (C), 3 cm in (B), 5 mm in (D), and 1 cm in (E).
RESEARCH |REPORTS
shore birds (22), and interdigital webbing has
been reported in theropod dinosaurs (29).
Reduction of the pelvic girdle and hindlimb and
the concomitant enhancement of axial-powered
locomotion are common among semiaquatic
vertebrates. The flexibility of the tail and the
form of the neural spines in Spinosaurus suggest
tail-assisted swimming. Like extinct and extant
semiaquatic reptiles, Spinosaurus used lateral
undulation of the tail, in contrast to the vertical
axial undulation adopted repeatedly by semi-
aquatic mammals (20,21).
The dorsal sailin Spinosaurus, the tallest
axial structure documented among dinosaurs,
has been argued to be a thermoregulatory sur-
face, a muscle- or fat-lined hump (30), or a dis-
play structure. Stromer (1) drew an analogy to
the skin-covered neural spines of the crested
chameleon, Trioceros cristatus (Fig. 4E). As in
T. cristatus,thesailofSpinosaurus is centered
over the trunk (Fig. 2A). The shape and position-
ing of the spine are also similar, and the base of
the neural spine is expanded anteroposteriorly,
with edges marked by ligament scars (Fig. 2E).
In Trioceros, a tendon of multisegmental axial
musculature attaches to the expanded base of
the neural spine (Fig. 4E). The upper portion of
the spine has sharp anterior and posterior edges,
is marked by fine vertical striae (Figs. 2E and 4D),
and is spaced away from adjacent spines, un-
lik e the broader, contiguous, paddle-shaped dorsal
spines of other spinosaurids (13). The striated
surface, sharp edges, and dense, poorly vascular-
ized internal bone of the spines suggest that they
were wrapped snugly in skin and functioned as
a display structure that would have remained
visible while swimming.
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ACKNOW LEDGMENT S
We thank C. Abraczinskas for final drafts of all text figures;
M. Auditore for discussions and drawings; T. Keillor, L. Conroy,
and E. Fitzgerald for image processing and modeling; R. Masek,
T. Keillor, E. Fitzgerald, and F. Bacchia for fossil preparation;
C. Straus, N. Gruszauskas, D. Klein, and the University of Chicago
Medical Center for computed tomographic scanning; M. Zilioli,
F. Marchesini, M. Pacini, E. Lamm, and P. Vignola for preparation of
histological samples; A. Di Marzio (Siemens Milano) and P. Biondetti
(Fondazione Ospedale Maggiore Istituto di Ricovero e Cura a
Carattere Scientifico, Milan) for computed tomography scanning and
rendering of MSNM V4047; and the Island Fund of the New York
Community Trust and National Geographic Society (grant
SP-13-12) for support of this research. N.I. was also supported by
NSF grant DBI-1062542. We also thank the embassy of the
Kingdom of Morocco in Washington, DC, for their continued
interest in this project. Skeletal measurements and geologic data
are included in the supplementary materials. The neotype is going to
be deposited at the Faculté des Sciences Aïn Chock (University of
Casablanca), Casablanca, Morocco.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/345/6204/1613/suppl/DC1
Supplementary Text
Figs. S1 to S8
Tables S1 to S5
References (3148)
15 July 2014; accepted 3 September 2014
10.1126/science.1258750
NEUROSCIENCE
A critical time window for dopamine
actions on the structural plasticity
of dendritic spines
Sho Yagishita,
1,2
Akiko Hayashi-Takagi,
1,2,3
Graham C.R. Ellis-Davies,
4
Hidetoshi Urakubo,
5
Shin Ishii,
5
Haruo Kasai
1,2
*
Animal behaviors are reinforced by subsequent rewards following within a narrow time
window. Such reward signals are primarily coded by dopamine, which modulates the
synaptic connections of medium spiny neurons in the striatum. The mechanisms of the
narrow timing detection, however, remain unknown. Here, we optically stimulated
dopaminergic and glutamatergic inputs separately and found that dopamine promoted
spine enlargement only during a narrow time window (0.3 to 2 seconds) after the
glutamatergic inputs. The temporal contingency was detected by rapid regulation of
adenosine 3,5-cyclic monophosphate in thin distal dendrites, in which protein-kinase
A was activated only within the time window because of a high phosphodiesterase
activity. Thus, we describe a molecular basis of reinforcement plasticity at the level of
single dendritic spines.
Animal behaviors are reinforced only when
rewarded shortly after a motor or sensory
event (1,2). The neocortex, hippocampus,
and amygdala process the sensorimotor
signals and send glutamatergic synaptic out-
put to the striatum (3), where connections can
be modified by Hebbian learning mechanisms,
such as spike-timing-dependent plasticity (STDP)
(4). Animals learn to associate the sensorimotor
signals with subsequent rewards through rein-
forcement of the neuronal circuits involving do-
pamine (57). Despite its importance, this narrow
timing detection has never been demonstrated at
the cellular level and might be ascribed to neural
network properties (6,8).
Dendritic spine morphology is correlated with
spine function (9), and dendritic spines enlarge
during long-term potentiation in the cortices
(1012). We examined the effects of dopamine
on the structural plasticity in striatal medium
spiny neurons (MSNs). Results show that do-
pamine affected spine structural plasticity in a
narrow time window consistent with behav-
ioral conditioning (5). Functional imaging revealed
the molecular interrelationships between the re-
inforcement and Hebbian plasticity.
We investigated dopamine actions on glutama-
tergic synapses on MSNs using optogenetics and
1616 26 SEPTEMBER 2014 VOL 345 ISSUE 6204 sciencemag.org SCIENCE
1
Laboratory of Structural Physiology, Center for Disease
Biology and Integrative Medicine, Faculty of Medicine, The
University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan.
2
Core Research for Evolutional Science and Technology,
Japan Science and Technology Agency, Japan Science and
Technology Agency, 4-1-8 Honcho, Kawaguchi, Saitama
332-0012, Japan.
3
Precursory Research for Embryonic
Science and Technology, Japan Science and Technology
Agency, Japan Science and Technology Agency, 4-1-8
Honcho, Kawaguchi, Saitama 332-0012, Japan.
4
Department
of Neuroscience, Mount Sinai School of Medicine, New York,
NY 10029, USA.
5
Integrated Systems Biology Laboratory,
Department of Systems Science, Graduate School of
Informatics, Kyoto University, Sakyo-ku, Kyoto 606-8501,
Japan.
*Corresponding author. E-mail: hkasai@m.u-tokyo.ac.jp
RESEARCH |REPORTS
  • ... Locomotion in water is a major point of contention 10,11 , because no unambiguous evidence for a plausible mode of propulsion has been presented. Furthermore, our understanding of the anatomy and ecology of this highly derived theropod has been hampered because only one associated Spinosaurus skeleton exists, with all other associated remains having been destroyed in World War II 7 . The posterior portion of the skeleton and the caudal vertebral series in particular, which has the potential to shed light on likely adaptations for aquatic locomotion, has until now been poorly understood 12 . ...
    ... Here we describe a nearly complete and partially articulated tail of a subadult individual of S. aegyptiacus (accession code Faculté des The skeleton represents, to our knowledge, the most complete dinosaur known from the Kem Kem beds 21,22 and the most complete skeleton of a Cretaceous theropod known from mainland Africa (Supplementary Information section 2). As we show here, the tail forms part of the neotype of S. aegyptiacus 7 and was found in direct juxtaposition to the remainder of the skeleton (Extended Data Fig. 3). The newly recovered material confirms the previous conclusion 7 that a single subadult individual is preserved at the site; over 90% of the new material was recovered during field excavations in late 2018, and then digitally recorded (Extended Data Figs. ...
    ... The skeletal remains of Spinosaurus (Supplementary Information) from the Kem Kem beds-composed of sediments deposited in a major fluvio-deltaic system 7 that have yielded a diverse vertebrate assemblage 27 -provide further insights into the ecology of this dinosaur. The composition of the ecosystem represented by the Kem Kem assemblage is highly atypical, containing a rich freshwater fauna dominated by fishes (including lungfish and large-to-very-large sawfish and coelacanths 27 ), a diverse range of crocodyliforms 28 and several giant predatory dinosaurs 7,22 . The seemingly anomalous occurrence in the same deposits of several large-bodied predators but few terrestrial herbivores is partially explained by the largely aquatic and probably piscivorous lifestyle of Spinosaurus, which considerably expands the morphological and ecological disparity of Kem Kem tetrapods 7,29 . ...
    Article
    Full-text available
    In recent decades, intensive research on non-avian dinosaurs has strongly suggested that these animals were restricted to terrestrial environments1. Historical proposals that some groups, such as sauropods and hadrosaurs, lived in aquatic environments2,3 were abandoned decades ago4–6. It has recently been argued that at least some of the spinosaurids—an unusual group of large-bodied theropods of the Cretaceous era—were semi-aquatic7,8, but this idea has been challenged on anatomical, biomechanical and taphonomic grounds, and remains controversial9–11. Here we present unambiguous evidence for an aquatic propulsive structure in a dinosaur, the giant theropod Spinosaurus aegyptiacus7,12. This dinosaur has a tail with an unexpected and unique shape that consists of extremely tall neural spines and elongate chevrons, which forms a large, flexible fin-like organ capable of extensive lateral excursion. Using a robotic flapping apparatus to measure undulatory forces in physical models of different tail shapes, we show that the tail shape of Spinosaurus produces greater thrust and efficiency in water than the tail shapes of terrestrial dinosaurs and that these measures of performance are more comparable to those of extant aquatic vertebrates that use vertically expanded tails to generate forward propulsion while swimming. These results are consistent with the suite of adaptations for an aquatic lifestyle and piscivorous diet that have previously been documented for Spinosaurus7,13,14. Although developed to a lesser degree, aquatic adaptations are also found in other members of the spinosaurid clade15,16, which had a near-global distribution and a stratigraphic range of more than 50 million years14, pointing to a substantial invasion of aquatic environments by dinosaurs. Discovery that the giant theropod dinosaur Spinosaurus has a large flexible tail indicates that it was primarily aquatic and swam in a similar manner to extant tail-propelled aquatic vertebrates.
  • ... A notable feature of the Kem Kem assemblage is the taxonomic, numerical and ichnological dominance of theropods among dinosaurs. Some authors regard this as an accurate reflection of the dominance of theropods in the fauna during the Cenomanian (Russell 1996, Mahler 2005, Läng et al. 2013, Ibrahim et al. 2014a, Ibrahim et al. 2014b, Ibrahim et al. 2016. Others have suggested that the perceived diversity (Dyke 2010) and abundance (McGowan and Dyke 2009, Dyke 2010) of theropods is a result of geological or collecting biases. ...
    ... The geological and paleontological evidence reviewed in this report bears directly on these controversies. Lapparent de Broin 2016, Young et al. 2017, pterosaurs (Wellnhofer and Buffetaut 1999, Mader and Kellner 1999, Ibrahim et al. 2010, Rodrigues et al. 2011, Martill and Ibrahim 2015, Jacobs et al. 2019, non-avian dinosaurs (Lavocat 1948, 1954b, Buffetaut 1989, Sereno et al. 1996, Russell 1996, Milner 2003, Amiot et al. 2004, Novas et al. 2005a, Mahler 2005, Dal Sasso et al. 2005, Ibrahim at al. 2014a, Ibrahim et al. 2014b, Evers et al. 2015, Ibrahim et al. 2016, Chiarenza and Cau 2016, and a possible avian . ...
    ... In the predominant fluvial facies, isolated and transported fossils are the norm. Only three associated partial dinosaur skeletons have been recovered, the diplodocoid sauropod Rebbachisaurus garasbae (Lavocat 1954b, Wilson and and the theropods Deltadromeus agilis (Sereno et al. 1996) and Spinosaurus aegyptiacus (Ibrahim et al. 2014b). In addition, one associated dinosaur skull pertaining to the large theropod Carcharodontosaurus saharicus has been recovered (Sereno et al. 1996). ...
    Article
    Full-text available
    The geological and paleoenvironmental setting and the vertebrate taxonomy of the fossiliferous, Cenomanian-age deltaic sediments in eastern Morocco, generally referred to as the “Kem Kem beds”, are reviewed. These strata are recognized here as the Kem Kem Group, which is composed of the lower Gara Sbaa and upper Douira formations. Both formations have yielded a similar fossil vertebrate assemblage of predominantly isolated elements pertaining to cartilaginous and bony fishes, turtles, crocodyliforms, pterosaurs, and dinosaurs, as well as invertebrate, plant, and trace fossils. These fossils, now in collections around the world, are reviewed and tabulated. The Kem Kem vertebrate fauna is biased toward largebodied carnivores including at least four large-bodied non-avian theropods (an abelisaurid, Spinosaurus, Carcharodontosaurus, and Deltadromeus), several large-bodied pterosaurs, and several large crocodyliforms. No comparable modern terrestrial ecosystem exists with similar bias toward large-bodied carnivores. The Kem Kem vertebrate assemblage, currently the best documented association just prior to the onset of the Cenomanian-Turonian marine transgression, captures the taxonomic diversity of a widespread northern African fauna better than any other contemporary assemblage from elsewhere in Africa. Keywords Africa, Cretaceous, dinosaur, Gara Sbaa Formation, Douira Formation, paleoenvironment, vertebrate
  • ... Limestone scree from the overlying Akrabou Formation often obscures the lower portion of the escarpment (Jacobs et al., 2019) and thus exposures of the Kem Kem beds can be sparse, despite the length of the outcrop. Most of the lower part of the sequence comprises fluvial cross-bedded, generally fine sandstones, with thinner beds of mudstones and intraformational mud-flake conglomerates containing rip up clasts, quartz and sandstone pebbles often with abundant bones and teeth (Ibrahim et al., 2014b). Vertebrate remains occur primarily in the mud-flake conglomerate beds but are occasionally reported from intervening horizons (Ibrahim et al., 2014b). ...
    ... Most of the lower part of the sequence comprises fluvial cross-bedded, generally fine sandstones, with thinner beds of mudstones and intraformational mud-flake conglomerates containing rip up clasts, quartz and sandstone pebbles often with abundant bones and teeth (Ibrahim et al., 2014b). Vertebrate remains occur primarily in the mud-flake conglomerate beds but are occasionally reported from intervening horizons (Ibrahim et al., 2014b). ...
    ... Remains of snakes have also been reported, including Norisophis (Klein et al., 2017),Simoliophis (Rage and Dutheil, 2008) and Lapparentophis (Vullo, 2019). Kem Kem beds dinosaurs include the theropods Spinosaurus, Carcharodontosaurus and Deltadromeus, whilst sauropods are represented by Rebbachisaurus and at least one additional unnamed taxon (Sereno et al., 1996;Cau et al., 2012;Mannion and Barrett, 2013;Ibrahim et al., 2014bIbrahim et al., , 2016Wilson and Allain, 2015). ...
    Article
    Pterodactyloid pterosaurs underwent a diversification in the Late Jurassic and Early Cretaceous, followed by a major turnover event in the mid-Cretaceous, when ornithocheiroids and basal azhdarchoids were replaced by pteranodontids, nyctosaurids and azhdarchids in the latest Cretaceous. However, precise patterns of turnover are obscured by the incompleteness of the pterosaur fossil record. Fossils from the middle Cretaceous Kem Kem beds of Morocco (?Albian –Cenomanian) have helped shed light on the diversity of pterosaurs from this time and provide a window into the diversity of a continental pterosaur assemblage from this critical transitional period. Two toothed pterosaurs, the ornithocheirids Siroccopteryx moroccensis and Coloborhynchus fluviferox, have been reported from the Kem Kem beds. Here, we report a partial mandible and two premaxillae representing three additional taxa of toothed pterosaurs. The mandibular symphysis closely resembles that of Anhanguera piscator from the Romualdo Member of the Santana Formation of Brazil in the arrangement and spacing of the alveoli, the weak anterior upturn of the jaw, and the ventral crest. One premaxilla closely resembles that of the ornithocheirid Ornithocheirus simus from the Cambridge Greensand Formation of eastern England. A second premaxilla is referred to Coloborhynchus, bearing similarities to C. clavirostris from the Hastings Group of southern England, and C. fluviferox from the Kem Kem beds of Morocco. In total, the Kem Kem pterosaur fauna includes at least nine species, of which three are ornithocheirids. The Kem Kem assemblage supports the idea that toothed pterosaurs remained diverse during the mid Cretaceous before disappearing from post-Cenomanian strata.
  • ... A virtual environment, unlike using physical models, allows assembling a number of bones only limited by computation power without the need for supports. Also, virtual skeletal mounts using high resolution scans of the actual fossils (Ibrahim et al. 2014;Lacovara et al. 2014;Mallison 2010b, c) allow creating mounts faithful to the original skeletons, in contrast with building virtual models manually from pictures or drawings of specimens (Stevens 2002;Stevens and Parrish 1999) which is not only time consuming, but also leading to huge differences in shape between the model and the real fossil bones (Mallison 2007). Finally, taphonomic compression or shearing, one large caveat of mounting real fossil bones or casts (which may explain the disarticulation of Diplodocus carnegii posterior cervical vertebrae), can be easily solved in virtual environments (Tschopp et al. 2013;Vidal and Díaz 2017). ...
    ... 1. Mounting virtual skeletons using bones manually modeled from pictures or drawings of fossils may accumulate errors derived from preconceived notions present in photographs and/or drawings, as happened with skeletal reconstructions of Plateosaurus (Mallison 2007, c). 2. Virtual skeletons may also disarticulate bones, creating postures which require disarticulated bones (which also help in spreading preconceived notions). 3. Mounting virtual composite skeletons may render chimaeras, as could be the case for the virtual Spinosaurus aegyptiacus (Ibrahim et al. 2014) if some of the bones used in its construction belong to Sigilmassaurus or a yet unnamed spinosaur (Evers et al. 2015). ...
    Article
    Fossil skeletal mounts are more than popular attractions at paleontological exhibitions. Thorough History they have proven, when properly mounted, to be great devices for evaluating paleobiological hypotheses otherwise untestable. Nevertheless, mounting skeletons based on preconceived notions or looking for spectacularity has also contributed to spark a lot of scientific debate for decades. This work reviews some historical and recent cases on how skeletal mounting of sauropodomorph dinosaurs, physical or virtual, has resulted as hypothesis testing device or as a vehicle for false hypotheses to spread. Skeletal mounts can be valid hypothesis testing devices when following strict rigorous and repeatable protocols. Some criteria for evaluating previously existing mounts or executing new ones are proposed.
  • ... The mid-Cretaceous (upper Albian-lower Cenomanian, Vullo, 2019) Kem Kem Group (Ibrahim et al., 2020) of south-east Morocco, is well known for it's high abundance and diversity of terrestrial, aquatic and volant vertebrates. The Kem Kem Group (Ifezouane and Aoufous formations) represents a fluvial facies succession composed of moderate to well-sorted point-bar sandstones and floodplain mudstones (Ibrahim et al., 2014a;Jacobs et al., 2019;Fig. 1). ...
    ... 1). The Kem Kem Group is best known for large theropod dinosaurs, most notably Carcharodontosaurus and the semi-aquatic Spinosaurus aegyptiacus (Russell, 1996;Dal Sasso et al., 2005;Ibrahim et al., 2014a). However, fossil fish remains (Osteichthyes and Chondrichthyes) are perhaps the most abundant fossils in these fluvial deposits and are demonstrably highly diverse with many major Cretaceous fish groups represented . ...
    Article
    Full-text available
    Pycnodont fishes (Actinopterygii, Pycnodontomorpha) contributed a major role to many ichthyological assemblages in the Mesozoic, however their occurrence in the continental mid-Cretaceous Kem Kem beds of Morocco was only briefly noted by Sereno et al., (1996) but were not described. Here we describe the first diverse pycnodont assemblage in the Kem Kem beds of the Tafilalt region, based mainly on recent collecting. Pycnodont remains are represented by rare, mostly incomplete fragments of vomerine and prearticular dentitions, but despite their rarity, they are surprisingly diverse with four morphotypes represented, including two new forms: Neoproscinetes africanus sp. nov. and Agassizilia gen. nov. From a sample of eight specimens, four species are recorded, three of which are new. The palaeoecology, taphonomy and biostratinomy of the specimens is discussed in the context of their occurrence in a predominantly freshwater sequence. Comparisons are made with the pycnodont assemblage of the approximately coeval Santana Group (Brazil) which contains taxa with similarities to the new Moroccan pycnodonts. These new pycnodont taxa increase the already diverse assemblage of the Kem Kem beds ichthyofauna.
  • ... Recently, using computed tomography, related internal structures were proposed for different marine reptiles, such as plesiosaurs (Foffa et al. 2014;O'Gorman and Gasparini 2013), ichthyosaurs (Kear 2005;Lomax et al. 2019, and references therein), and crocodylomorphs (George and Holliday 2013;Leicht and Catania 2012;Soares 2002), and were thought to belong to branches of the trigeminal nerve as well, serving to enhance skin sensitiveness. Furthermore, even some terrestrial dinosaurs exhibited similar structures (Barker et al. 2017;Cau et al. 2017;Ibrahim et al. 2014), suggesting that specialized sensory organs were convergently acquired, and were more widely distributed than previously thought. ...
    Article
    Full-text available
    Mosasaurs were a cosmopolitan group of marine squamate reptiles that lived during the Late Cretaceous period. Tylosaurinae mosasaurs were characterized for having an edentulous rostrum anterior to the premaxillary teeth. External morphology of the snout of the tylosaurine Taniwhasaurus antarcticus from the Upper Cretaceous beds at James Ross Island (Antarctic Peninsula) shows a complex anatomy with diverse large foramina and bone sculpture. A computed tomography scan of the Taniwhasaurus rostrum revealed a complex internal neurovascular system of branched channels in the anteriormost part of the snout. Systems like this are present in extant aquatic vertebrates such as cetaceans and crocodiles to aid them with prey detection, and are inferred to have functioned in a similar manner for several extinct reptile clades such as plesiosaurs and ichthyosaurs. Thus, it is probable that Taniwhasaurus also was able to detect prey with an enhanced neural system located in its rostrum. This condition may be more widespread than previously thought among mosasaurs and other marine reptiles.
  • ... The majority of the similarities with some maniraptoriforms are homoplastic convergences (a phenomenon widespread among theropod dinosaurs, see Holtz, 2001). At least seven of the halszkaraptorine novelties are convergently acquired by spinosaurids, and are integrated in a semiacquatic and piscivorous ecology (Charig & Milner, 1997;Ibrahim et al., 2014;Cau et al., 2017; Table 1). One of these features, reported here for the first time, is the "festooning pattern" in the upper dentition size variation, which recalls semi-aquatic crocodilians (Charig & Milner, 1997;Dal Sasso et al., 2005;Pol, Turner & Norell, 2009). ...
    Article
    Full-text available
    The dromaeosaurid theropod Halszkaraptor escuilliei is characterized by several unusual features absent in other paravians, part of which has been interpreted as diagnostic of a novel lineage adapted to a semiaquatic ecology. Recently, these evolutionary and ecological interpretations have been challenged, and Halszkaraptor has been claimed to be a transitional form between non-dromaeosaurid maniraptoriforms and other dromaeosaurids: following that reevaluation, its peculiar body plan would represent the retention of several maniraptoran plesiomorphies, lost among other dromaeosaurids, and not an adaptation to a novel ecology. This alternative scenario is here carefully investigated and tested. It is shown that most statements supporting this scenario are based on misinterpretation of anatomical traits and bibliography. Once these statements have been corrected, character state transition optimization over a well-supported phylogenetic framework indicates that the large majority of the peculiar features of the Halszkaraptor lineage are derived novelties acquired by the latter after its divergence from the last ancestor shared with eudromaeosaurs, and thus are not maniraptoriform plesiomorphies. At least seven novelties of the Halszkaraptor lineage are convergently acquired with spinosaurids, and are integrated in semiaquatic adaptations: one of these is reported here for the first time. The amount of morphological divergence of Halszkaraptorinae from the ancestral dromaeosaurid condition is comparable to those of Microraptorinae and Velociraptorinae. Among extant taxa, the sawbills (Mergini, Anseriformes) show the closest ecomorphological similarity with the peculiar body plan inferred for Halszkaraptor. The halszkaraptorine bauplan is thus confirmed as a derived amphibious specialization, and does not represent a "transitional" stage along the evolution of dromaeosaurids.
  • ... Moreover, in recent decades, several more sauropod remains have been (re)described (e.g. Ibrahim et al., 2014). The carnivorous vertebrate fauna seems to be overrepresented, especially in the Kem Kem beds of Morocco (see Läng et al., 2013). ...
  • ... Moreover, in recent decades, several more sauropod remains have been (re)described (e.g. Ibrahim et al., 2014). The carnivorous vertebrate fauna seems to be overrepresented, especially in the Kem Kem beds of Morocco (see Läng et al., 2013). ...
  • Book
    Full-text available
    Hastings & District Geological Society Journal, Vol.20, December 2014 (Low Resolution) CONTENTS: 2014 Officials and Committee . . . p.1 // Ecclesbourne Glen, Hastings - by Ken Brooks . . . p.2 // Sussex Mineral Society goes to Maine, USA - by Trevor Devon . . . p.5 // Bexhill dinosaur - an update - by Peter and Joyce Austen . . . p.8 // Report on the visit by a group of HDGS members to the Bexhill to Hastings Link Road - by Jim Simpson . . . p.10 // Photographs of HDGS visit behind the scenes at the Natural History Museum - June 2014 . . . p.16 // Geology of The Azores, Portugal - by Margaret A Dale . . . p.17 // Sussex Mineral Show - Saturday, 14th November 2015 . . . p.19 // 200 years of William Smith’s momentous map - by Anthony Brook . . . p.20 // William Smith and the Castle Hill section - by Anthony Brook . . . p.22 // Geology Group Beach Barbecue - by Kay Wilks . . . p.22 // HDGS/GA field meeting: Covehurst Bay to Fairlight Cove, Hastings - by Ed Jarzembowski, Peter Austen and Ken Brooks . . . p.23 // Cliff fall at Rock-a-Nore, Hastings . . . p.25 // Devonian - “The Age of Fishes” - reported by Peter and Joyce Austen . . . p.26 // Book review - Geology and Fossils of the Hastings Area (Second edition) - reviewed by Chris Darmon in Down to Earth . . . p.36 // Geologists’ Association Field Meetings - 2015 . . . p.36 // Cliff recedes at Birling Gap - by Joyce Austen . . . p.37 // Palaeontology in the News - edited by Peter and Joyce Austen . . . p.38 // Obituary - Nancy Margaret Wagner, 1907-2014 . . . p.50 // Obituary - Martin Bluhm, 1933-2014 . . . p.51 // Minutes of the AGM - 8th December 2013 . . . p.52 // Statement of Income & Expenditure and Balances for the Year Ending 31st December 2013 . . . p.55.
  • Article
    The 'Gres rouges infracenomaniens' of southern Morocco, possibly of Albian age, contain evidence of one of the most diversified dinosaur assemblages known from Africa, including a relatively long-necked species of Spinosaurus and abundant but isolated bones of a peculiar theropod ('Spinosaurus B' of Stromer 1934). Also preserved are the oldest records of abelisaurids and among the oldest records of titanosaurids in Africa. Bones of infantile didnosaurs are present. The assemblage resembles that of the Bahariya Formation more than that of Gadoufaoua, possibly because of a trophic dependence upon large, freshwater fishes. It was more closely linked zoogeographically to South America than to North America.
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  • Article
    Noasauridae is a clade of ceratosaurian theropods that evolved small body size independently of other non-avian theropods. The best-preserved and most complete noasaurid is Masiakasaurus knopfleri from the Maastrichtian-aged Maevarano Formation in Madagascar. An abundance of skeletal material from several individuals spanning a wide range of ontogeny makes Masiakasaurus an ideal candidate for the analysis of growth. We histologically sampled a growth series of elements consisting of four femora and three tibiae. Bright-field and circularly polarized light microscopy were used to distinguish between slowly and rapidly growing forms of bone. To simultaneously estimate age at death and reconstruct growth trajectories, we measured the perimeters of growth lines in each specimen and fitted models to these data using a novel application of mixed-effects regression. Our histological results show an external fundamental system in the largest tibial specimen and confirm that Masiakasaurus grew determinately, matured at small body size, and is not the juvenile form of a larger-bodied theropod. Parallel-fibered bone is unusually prominent and suggests relatively slow growth. Moreover, our quantitative analysis shows that the average individual took about 8–10 years to get to the size of a large dog. Although Masiakasaurus grew 40% faster than crocodylians, it grew about 40% slower than comparably sized non-avian theropods. Slowed growth may have evolved as a means to minimize structural and maintenance costs while living in a semiarid and seasonally stressful environment. Dimorphism does not appear related to asymptotic size or growth rate but seems to reflect the degree of skeletal maturity.SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP
  • Article
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