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Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs

Authors:
Andrea Cau
Andrea Cau
Vincent Beyrand at University of Zurich
Vincent Beyrand
Dennis F. A. E. Voeten at Frisian Museum of Natural History
Dennis F. A. E. Voeten
  • Frisian Museum of Natural History
Vincent Fernandez at Natural History Museum, London
Vincent Fernandez
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Abstract and Figures

Maniraptora includes birds and their closest relatives among theropod dinosaurs. During the Cretaceous period, several maniraptoran lineages diverged from the ancestral coelurosaurian bauplan and evolved novel ecomorphologies, including active flight, gigantism, cursoriality and herbivory. Propagation X-ray phase-contrast synchrotron microtomography of a well-preserved maniraptoran from Mongolia, still partially embedded in the rock matrix, revealed a mosaic of features, most of them absent among non-avian maniraptorans but shared by reptilian and avian groups with aquatic or semiaquatic ecologies. This new theropod, Halszkaraptor escuilliei gen. et sp. nov., is related to other enigmatic Late Cretaceous maniraptorans from Mongolia in a novel clade at the root of Dromaeosauridae. This lineage adds an amphibious ecomorphology to those evolved by maniraptorans: it acquired a predatory mode that relied mainly on neck hyperelongation for food procurement, it coupled the obligatory bipedalism of theropods with forelimb proportions that may support a swimming function, and it developed postural adaptations convergent with short-tailed birds.
| H. escuilliei phylogenetic affinities and comparisons for its unique postcranial features. a-e, Dromaeosaurid synapomorphies in Halszkaraptor. a, Skull in occipital view. fm, foramen magnum; po, postorbital; pf, enlarged paraquadrate fenestra. b, Premaxilla and maxilla in lateral view. ep, elongate pre-antorbital part of maxilla; mf, dorsally placed maxillary fenestra. c, Mandible in lateral view. dm, dentary ventral and dorsal margins subparallel. d, Dentary tooth in lingual view. cd, concave distal margin of crown; ub, unconstricted crown base. e, Neck in ventrolateral view. na, neural arch extended to level of intercentral facet. f, Feet in extensor view. gm, ginglymoidal distal end of metatarsal II; sp, short and stout phalanges of second toe. g, Phylogenetic position of Halszkaraptor among Maniraptora, on the basis of parsimony analysis using TNT software 30 on two independently developed datasets 22 (for complete topologies and tree statistics, see Supplementary Information). h-j, Dorsal view of anterior cervical vertebrae of Cygnus (h), the fresh-water chelonian Araripemys 7 (i) and Halszkaraptor (j). These vertebrae share a combination of features: (1) elongate neural arches with reduced ridge-like neural spines; (2) merged postzygapophyses that form a lobate process; (3) ribs fused to vertebra; and (4) horizontally oriented zygapophyseal facets. Scale bars, 9 mm (a, c), 3 mm (b); 1 mm (d) and 30 mm (e, f).
| H. escuilliei phylogenetic affinities and comparisons for its unique postcranial features. a-e, Dromaeosaurid synapomorphies in Halszkaraptor. a, Skull in occipital view. fm, foramen magnum; po, postorbital; pf, enlarged paraquadrate fenestra. b, Premaxilla and maxilla in lateral view. ep, elongate pre-antorbital part of maxilla; mf, dorsally placed maxillary fenestra. c, Mandible in lateral view. dm, dentary ventral and dorsal margins subparallel. d, Dentary tooth in lingual view. cd, concave distal margin of crown; ub, unconstricted crown base. e, Neck in ventrolateral view. na, neural arch extended to level of intercentral facet. f, Feet in extensor view. gm, ginglymoidal distal end of metatarsal II; sp, short and stout phalanges of second toe. g, Phylogenetic position of Halszkaraptor among Maniraptora, on the basis of parsimony analysis using TNT software 30 on two independently developed datasets 22 (for complete topologies and tree statistics, see Supplementary Information). h-j, Dorsal view of anterior cervical vertebrae of Cygnus (h), the fresh-water chelonian Araripemys 7 (i) and Halszkaraptor (j). These vertebrae share a combination of features: (1) elongate neural arches with reduced ridge-like neural spines; (2) merged postzygapophyses that form a lobate process; (3) ribs fused to vertebra; and (4) horizontally oriented zygapophyseal facets. Scale bars, 9 mm (a, c), 3 mm (b); 1 mm (d) and 30 mm (e, f).
… 
| Morphometric analyses of aquatic adaptations in the Halszkaraptor forelimb. a, Binary plot of length ratios among manual digits I-III in aquatic and terrestrial sauropsids (n = 84): Halszkaraptor clusters with long-necked aquatic reptiles. b, Binary plot of principal components 2 and 3 from a morphometric analysis of ten skeletal characters of the forelimb and sternum in birds (n = 246; principal component 1 describes body size variation and is therefore not considered; see Supplementary Information): Halszkaraptor clusters with wingpropelled swimming birds. Silhouettes in a provided by D. Bonadonna and L. Panzarin.
| Morphometric analyses of aquatic adaptations in the Halszkaraptor forelimb. a, Binary plot of length ratios among manual digits I-III in aquatic and terrestrial sauropsids (n = 84): Halszkaraptor clusters with long-necked aquatic reptiles. b, Binary plot of principal components 2 and 3 from a morphometric analysis of ten skeletal characters of the forelimb and sternum in birds (n = 246; principal component 1 describes body size variation and is therefore not considered; see Supplementary Information): Halszkaraptor clusters with wingpropelled swimming birds. Silhouettes in a provided by D. Bonadonna and L. Panzarin.
… 
Example of data processed with texture enhancement and metallic-inclusion correction algorithms a, Virtual section or the original dataset. b, Detail of a. c, Virtual section from the dataset corrected for metallic inclusions. d, Detail of c. Histograms along the blue and red lines demonstrate how metallic inclusions prevent adjusting the contrast to focus on the bone–matrix contact. e, Virtual section along the longitudinal axis of the cranium on dataset corrected for metallic inclusions. f, Detail of e. g, Same virtual section as in e, on data processed with the texture enhancement algorithm. h, Detail of g. In the processed data (g, h), homogenous parts (for example, bone or plaster) appear dark and the sediment reveals features that were barely visible prior to processing (e, f).
Example of data processed with texture enhancement and metallic-inclusion correction algorithms a, Virtual section or the original dataset. b, Detail of a. c, Virtual section from the dataset corrected for metallic inclusions. d, Detail of c. Histograms along the blue and red lines demonstrate how metallic inclusions prevent adjusting the contrast to focus on the bone–matrix contact. e, Virtual section along the longitudinal axis of the cranium on dataset corrected for metallic inclusions. f, Detail of e. g, Same virtual section as in e, on data processed with the texture enhancement algorithm. h, Detail of g. In the processed data (g, h), homogenous parts (for example, bone or plaster) appear dark and the sediment reveals features that were barely visible prior to processing (e, f).
… 
Reduced strict consensus of the shortest trees found by the analysis of the second dataset a, Non-pennaraptoran taxa; b, Pennaraptora. Numbers adjacent to nodes indicate decay index values >1.
Reduced strict consensus of the shortest trees found by the analysis of the second dataset a, Non-pennaraptoran taxa; b, Pennaraptora. Numbers adjacent to nodes indicate decay index values >1.
… 
Sectional slices that illustrate the integrity of MPC-D102/109 a, Detail of anterior end of neck and posterior half of skull that shows continuity of the craniocervical transition. b, Detail of neck and skull that shows continuity between bones and matrix. c, Detail of proximal caudal series that shows the glued crack that crosses both matrix and bone (arrow), which confirms continuity between the sacrum and tail. d, Selected series of slices that show the continuity of bones and matrix along main slab. e, Overview of MPC-D102/109 indicating the curved virtual slice along a polyline (materialized above a 3D rendering) with slices at 5 mm on each side of this line every 1 mm. The line follows the axial column in order to show the continuity of the vertebral series. Scale bar, 70 mm. The renderings are generated using scan data that have been corrected for the absorbing metallic oxide infilling.
+9
Sectional slices that illustrate the integrity of MPC-D102/109 a, Detail of anterior end of neck and posterior half of skull that shows continuity of the craniocervical transition. b, Detail of neck and skull that shows continuity between bones and matrix. c, Detail of proximal caudal series that shows the glued crack that crosses both matrix and bone (arrow), which confirms continuity between the sacrum and tail. d, Selected series of slices that show the continuity of bones and matrix along main slab. e, Overview of MPC-D102/109 indicating the curved virtual slice along a polyline (materialized above a 3D rendering) with slices at 5 mm on each side of this line every 1 mm. The line follows the axial column in order to show the continuity of the vertebral series. Scale bar, 70 mm. The renderings are generated using scan data that have been corrected for the absorbing metallic oxide infilling.
… 
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21/28 DECEMBER 2017 | VOL 552 | NATURE | 395
LETTER doi:10.1038/nature24679
Synchrotron scanning reveals amphibious
ecomorphology in a new clade of bird-like dinosaurs
Andrea Cau1, Vincent Beyrand2,3, Dennis F. A. E. Voeten2,3, Vincent Fernandez2, Paul Tafforeau2, Koen Stein4, Rinchen Barsbold5,
Khishigjav Tsogtbaatar6, Philip J. Currie7 & Pascal Godefroit8
Maniraptora includes birds and their closest relatives among
theropod dinosaurs1–5. During the Cretaceous period, several
maniraptoran lineages diverged from the ancestral coelurosaurian
bauplan and evolved novel ecomorphologies, including active
flight2, gigantism3, cursoriality4 and herbivory5. Propagation X-ray
phase-contrast synchrotron microtomography of a well-preserved
maniraptoran from Mongolia, still partially embedded in the rock
matrix, revealed a mosaic of features, most of them absent among
non-avian maniraptorans but shared by reptilian and avian groups
with aquatic or semiaquatic ecologies6–14. This new theropod,
Halszkaraptor escuilliei gen. et sp. nov., is related to other enigmatic
Late Cretaceous maniraptorans from Mongolia
15,16
in a novel clade
at the root of Dromaeosauridae17. This lineage adds an amphibious
ecomorphology to those evolved by maniraptorans: it acquired a
predatory mode that relied mainly on neck hyperelongation for food
procurement, it coupled the obligatory bipedalism of theropods with
forelimb proportions that may support a swimming function, and it
developed postural adaptations convergent with short-tailed birds.
Theropoda Marsh, 1881
Maniraptora Gauthier, 1986
Dromaeosauridae Matthew and Brown, 1922
Halszkaraptorinae subfam. nov.
Definition. The most inclusive clade that contains Halszkaraptor
escuilliei gen. et sp. nov., but not Dromaeosaurus albertensis, Unenlagia
comahuensis, Saurornithoides mongoliensis or Vu ltur g r yph u s. Taxa
included: Halszkaraptor escuilliei, Hulsanpes perlei15 and Mahakala
omnogovae16. Type species: Halszkaraptor escuilliei.
Diagnosis. Long-necked dromaeosaurids with proximal caudal
vertebrae that have horizontally oriented zygapophyses and prominent
zygodiapophyseal laminae; flattened ulna with a sharp posterior margin;
metacarpal III shaft transversely as thick as that of metacarpal II;
ilium with a shelf-like supratrochanteric process; posterodistal
surface of femoral shaft with an elongate fossa bound by a lateral crest;
proximal half of metatarsal III unconstricted and markedly convex
anteriorly.
Halszkaraptor escuilliei gen. et sp. nov.
Et y m ology. Halszka, a Latinized form of archaic Polish Halżka, honours
Halszka Osmólska (1930–2008) for her contributions to theropod
palaeontology, which include the description of the first halszkarap-
torine species found (Hulsanpes perlei)15; raptor, ‘robber’ (Latin). The
specific name escuilliei refers to François Escuillié, who returned the
poached holotype to Mongolia.
Holotype. MPC (Institute of Paleontology and Geology, Mongolian
Academy of Sciences, Ulaanbaatar, Mongolia) D-102/109 (Figs 1, 2,
3a–f, Extended Data Figs 2–8, Supplementary Table 1); an articulated
and almost complete skeleton preserved three-dimensionally.
Locality and horizon. Bayn Dzak Member, Djadokhta Formation
(Campanian, ~ 75–71 Mya), Ukhaa Tolgod, Mongolia (see
Supplementary Information).
Diagnosis. Autapomorphies are marked by asterisks; differential
diagnosis can be found in Supplementary Information. Platyrostral
premaxilla that forms 32% of snout length* and bears 11 teeth* ; external
naris posterior to the premaxillary oral margin; rod-like jugal with an
ascending process excluded from the orbital margin that forms only
10% of the postorbital bar* ; rod-like ventral ramus of the postorbital;
22 presacral vertebrae; neck forms 50% of snout–sacrum length* ;
absence of epipophyses* ; ridge-like cervical neural spines restricted
to the 2nd–5th vertebrae* ; postzygapophyses on cervicals 2–5 are
fused medially and form single lobate processes* ; pleurocoels restricted
to cervicals 7–9; tuber-like neural spines in tail are restricted to the
1st–3rd vertebrae* ; proximal-most chevrons large and pentagonal* ;
transition point in 7th–8th caudals; 3rd finger longer than 2nd; elongate
pedal phalanx III-1 is 47% of the length of metatarsal III* .
We performed multi-resolution scanning at the European
Synchrotron Radiation Facility using BM05 and ID19 beamlines;
this revealed all the elements that were still embedded in matrix
and demonstrated the integrity of the specimen (Supplementary
Information, Extended Data Figs 1–3). Histological analysis indi-
cates that MPCD-102/109 was a subadult individual (Supplementary
Information, Extended Data Figs 4, 5). The platyrostral premaxilla
with a dorsolaterally oriented external naris that is retracted beyond
the oral margin is unique among theropods, although in its elonga-
tion, the premaxilla is similar to those of spinosaurids8 (Fig. 2a–g,
Extended Data Figs 6, 8). A hypertrophied network of neurovascular
chambers penetrates throughout the premaxilla. This condition
is also seen in aquatic reptiles, such as plesiosaurs12 and crocodiles
(Fig. 2e, f, Extended Data Fig. 8), whereas in other theropods this neuro-
vascular network resides exclusively in the lateral half of the premaxilla13.
Each premaxilla bears 11 teeth (Fig. 2g, Extended Data Figs 6, 7),
which is the highest number found in any dinosaur. Spinosaurids and
Pelecanimimus approach Halszkaraptor in having six or seven premaxil-
lary teeth
8
, whereas most theropods have four. Both the maxilla and
the dentary bear 20–25 teeth; this is comparable to the condition seen
in unenlagiines
17
and baryonychines
8
. Although some maniraptori-
forms carry a total of over 30 small maxillary and/or dentary teeth
5
,
most theropods have fewer than 20. The heterodont dentition of
Halszkaraptor involves closely packed premaxillary teeth with long
roots and incisiviform crowns, and a labiolingually compressed pos-
terior dentition with shorter roots and concave distal crown margins
(Fig. 3d, Extended Data Fig. 7). All teeth lack serrations, as is the
case in most paravians7, spinosaurines8 and a few other theropods.
Synchrotron scanning revealed a delayed replacement pattern in the
anterior dentition14, whereas the majority of the posterior teeth are
associated with a replacement tooth.
1Geological and Palaeontological Museum ‘Giovanni Capellini’, I-40126 Bologna, Italy. 2European Synchrotron Radiation Facility, F-38043 Grenoble, France. 3Department of Zoology and
Laboratory of Ornithology, Palacký University, CS-40220 Olomouc, Czech Republic. 4Earth System Science – AMGC Vrije Universiteit Brussel, B-1050 Brussels, Belgium. 5Palaeontological Center,
Mongolian Academy of Sciences, Ulaanbaatar 201-351, Mongolia. 6Institute of Palaeontology and Geology, Mongolian Academy of Sciences, Ulaanbaatar 210-351, Mongolia. 7Department of
Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada. 8Directorate Earth & History of Life, Royal Belgian Institute of Natural Sciences, B-1000 Brussels, Belgium.
© 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
... The most complete bone of Diuqin is the left humerus, which is missing only parts of the proximal end and deltopectoral crest. There are no synapomorphies in the humerus of unenlagiines described by previous authors [14,17,83]. Nevertheless, that of Diuqin can be unequivocally assigned to Unenlagiinae based on the following combination of characters: (1) deltopectoral crest proximodistally short with respect to the humerus as a whole (as in the Buitreraptor holotype and Unenagia); (2) presence of a distolateral ridge on the lateral surface of the deltopectoral crest (as in Buitreraptor and U. comahuensis); ...
... The crown base lacks the constriction observed in several troodontids, which also generally have much larger, hooked denticles [99]. The presence of denticles and transverse undulations in MUCPv 1557 precludes its assignment to halszkaraptorine or unenlagiine dromaeosaurids [58,83], whereas the absence of longitudinal flutes/ridges and the presence of transverse undulations rules out Microraptorinae as well [99]. Also, there are several differences with eudromaeosaurians; for instance, the denticles are not hook-shaped as in Atrociraptor marshalli and Saurornitholestes langstoni, nor are there lateral ridges as in several other species (e.g., Acheroraptor temertyorum, Bambiraptor feinbergi, Linheraptor exquisitus, Velociraptor mongoliensis) [99]. ...
... The traces present on the distal humerus of MUCPv 1401 show inward-collapsed bone fragments with smooth surfaces, without any sign of furrows or crests that might have been made by enamel ridges. Moreover, several works [58,83,139] have proposed that unenlagiines might have been piscivorous, although Gianechini et al. [140] considered these paravians to have been primarily terrestrial predators. ...
Diuqin lechiguanae gen. et sp. nov., a new unenlagiine (Theropoda: Paraves) from the Bajo de la Carpa Formation (Neuquén Group, Upper Cretaceous) of Neuquén Province, Patagonia, Argentina
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... However Dromaeosauridae, the quintessential "raptors", have traditionally been painted with a broad brush as medium-sized, swift-moving macropredators [8,9]. Recently, some key specimens [10,11] have revealed that the characteristic ecological diversity of Theropoda is also reflected within Dromaeosauridae, but this has yet to be investigated quantitatively and with respect to their evolutionary history. ...
... Dromaeosaurids purportedly had a broad range of cranial morphology [10,11,24]. Different species also cohabitated in palaeoecosystems with diverse climates and environments [22,[25][26][27], implying diverse niches to limit competition with one another. ...
... However, we contest that this condition is indicative of aquatic predation. The source that [10] cites claiming platyrostry is indicative of piscivory [35] does not, in fact, make this claim. The relevant section describes longirostry (anteroposteriorly long and mediolaterally narrow rostrum) with a terminal rosette (ovoid mediolateral broadening of premaxilla), not platyrostry: "The jaws are long and very narrow from side to side; they are expanded horizontally at the anterior end […] this spatulate expansion forms a 'terminal rosette' , not unlike the corresponding region of the skull of a modern gavial" [35 , p.61]. ...
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Non-avialan theropod dinosaurs had diverse ecologies and varied skull morphologies. Previous studies of theropod cranial morphology mostly focused on higher-level taxa or characteristics associated with herbivory. To better understand morphological disparity and function within carnivorous theropod families, here we focus on the Dromaeosauridae, ‘raptors’ traditionally seen as agile carnivorous hunters. We applied 2D geometric morphometrics to quantify skull shape, performed mechanical advantage analysis to assess the efficiency of bite force transfer, and performed finite element analysis to examine strain distribution in the skull during biting. We find that dromaeosaurid skull morphology was less disparate than most non-avialan theropod groups. Their skulls show a continuum of form between those that are tall and short and those that are flat and long. We hypothesise that this narrower morphological disparity indicates developmental constraint on skull shape, as observed in some mammalian families. Mechanical advantage indicates that Dromaeosaurus albertensis and Deinonychus antirrhopus were adapted for relatively high bite forces, while Halszkaraptor escuilliei was adapted for high bite speed, and other dromaeosaurids for intermediate bite forces and speeds. Finite element analysis indicates regions of high strain are consistent within dromaeosaurid families but differ between them. Average strain levels do not follow any phylogenetic pattern, possibly due to ecological convergence between distantly-related taxa. Combining our new morphofunctional data with a re-evaluation of previous evidence, we find piscivorous reconstructions of Halszkaraptor escuilliei to be unlikely, and instead suggest an invertivorous diet and possible adaptations for feeding in murky water or other low-visibility conditions. We support Deinonychus antirrhopus as being adapted for taking large vertebrate prey, but we find that its skull is relatively less resistant to bite forces than other dromaeosaurids. Given the recovery of high bite force resistance for Velociraptor mongoliensis, which is believed to have regularly engaged in scavenging behaviour, we suggest that higher bite force resistance in a dromaeosaurid taxon may reflect a greater reliance on scavenging rather than fresh kills. Comparisons to the troodontid Gobivenator mongoliensis suggest that a gracile rostrum like that of Velociraptor mongoliensis is ancestral to their closest common ancestor (Deinonychosauria) and the robust rostra of Dromaeosaurus albertensis and Deinonychus antirrhopus are a derived condition. Gobivenator mongoliensis also displays a higher jaw mechanical advantage and lower resistance to bite force than the examined dromaeosaurids, but given the hypothesised ecological divergence of troodontids from dromaeosaurids it is unclear which group, if either, represents the ancestral condition. Future work extending sampling to troodontids would therefore be invaluable and provide much needed context to the origin of skull form and function in early birds. This study illustrates how skull shape and functional metrics can discern non-avialan theropod ecology at lower taxonomic levels and identify variants of carnivorous feeding. Supplementary Information The online version contains supplementary material available at 10.1186/s12862-024-02222-5.
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... The positive constraints were included in the analysis to recover a backbone topology, aligning with the results of previous phylogenetic studies. These constraints encompassed non-neotheropod saurischians (Müller et al., 2018), non-averostran neotheropods (Ezcurra, 2017), Ceratosauria (Rauhut and Carrano, 2016; Wang (Carrano et al., 2012;Rauhut et al., 2012;, Tyrannosauroidea (Brusatte and Carr, 2016), Megaraptora (Aranciaga Rolando et al., 2019), and neocoelurosaurs (Cau et al., 2017). All dental material were analyzed together, treating each tooth as a separate operational taxonomic unit (OTU), following the protocol of cladistic analysis established in previous works (Young et al., 2019;Hendrickx et al., 2020;Meso et al., 2021;Berrocal-Casero et al., 2022). ...
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... To carry out the phylogenetic analyses, we followed the methodology detailed by [23,24] in the software TNT v1.5 [25], using a backbone tree topology and the positive constraint command, setting the six dental morphotypes as floating terminals. The topological tree was built based on the results of the phylogenetic analyses of [26] for non-neotheropodsaurischians, [27] for non-averostranneotheropods, [28,29] for Ceratosauria, [30][31][32] for noncoelurosauriantetanurans, [33] for Tyrannosauroidea, [34] for Megaraptora, [35] for neocoelurosaurs, and [36] for Alvarezsauria. The search strategy of analysis used a combination of the tree-search algorithms Wagner trees, TBR branch swapping, sectorial searches, Ratchet (perturbation phase stopped after 20 substitutions), and Tree Fusing (5 rounds), until 100 hits of the same minimum tree length were reached (n.b., the TNT command used is "xmult = hits 100 rss fuse 5 ratchet 20"). ...
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... All ordered characters were considered as such and the basally branching saurischian Herrerasaurus was used as the operational outgroup to root the trees. To recover a backbone topology that follows current phylogenetic consensus on theropod dinosaurs, we applied in the phylogenetic analysis performed on the dentition-based data matrix a topological constraint to the data (command "constrain = ") based on the results from Müller et al. (2018) for non-neotheropod Saurischia, Ezcurra (2017) for non-averostran Neotheropoda, Rauhut and Carrano (2016) and Wang et al. (2017) for Ceratosauria, Carrano et al. (2012), Rauhut et al. (2012), and for non-coelurosaurian Tetanurae, Brusatte and Carr (2016) for Tyrannosauroidea, and Cau et al. (2017) for non-tyrannosauroid Coelurosauria. Second and third analyses were then performed on the dentition-and crown-based data matrices, respectively, without constraints and whose resulting most parsimonious trees (MPTs) strongly depart from the general consensus on theropod classification. ...
A combined approach to identify isolated theropod teeth from the Cenomanian Kem Kem Group of Morocco: cladistic, discriminant, and machine learning analyses
Article
The Kem Kem Group of Southeastern Morocco, North Africa, is well known for theropod remains, especially isolated teeth. Here, a collection of isolated theropod teeth is assessed for diversity using a combination of linear discriminant, phylogenetic, and machine learning analyses for the first time. The results confirm earlier studies on Kem Kem theropod diversity, with teeth referred to Abelisauridae, Spinosaurinae, and Carcharodontosauridae. A single tooth is ascribed to a non-abelisauroid ceratosaur or a megaraptoran and may represent the enigmatic averostran Deltadromeus. Spinosaurine teeth are clearly differentiated by all three methodologies, whereas abelisaurid and carcharodontosaurid teeth could only be distinguished by the machine learning and phylogenetic analyses. This study shows that a combination of independent methods is most effective at providing strong evidence on theropod dental diversity in a particular assemblage, and that cladistic and machine learning analyses are the most reliable approaches to identify isolated dinosaur teeth. The methodology used here is likely to yield results in other dinosaur assemblages where isolated teeth are more abundant than body fossils.
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... [26]and [27]for Ceratosauria, [28]and [29,30]for non-coelurosauriantetanurans, [31]for Tyrannosauroidea, [32]for Megaraptora, [33]for neocoelurosaurs, and [34]for Alvarezsauria. The search strategy of analysis used a combination of the tree-search algorithms Wagner trees, TBR branch swapping, sectorial searches, Ratchet (perturbation phase stopped after 20 substitutions), and Tree Fusing (5 rounds), until 100 hits of the same minimum tree length were reached (n.b., the TNT command used is "xmult = hits 100 rss fuse 5 ratchet 20"). ...
Shed teeth from Portezuelo Formation at Sierra del Portezuelo reveal a higher diversity of predator theropods during Turonian-Coniacian times in northern Patagonia
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Full-text available
  • Feb 2024
The study of thirty-two shed crowns from the Portezuelo Formation (middle Turonian-late Coniacian) at the Sierra del Portezuelo locality, reveals six distinct tooth morphotypes identified through cladistic, discriminant, and cluster analyses. Two morphotypes were identified as belonging to Megaraptoridae, three to Abelisauridae, one to Abelisauroidea, and one to Alvarezsauridae. Additionally, two of the morphotypes exhibit a combination of dental features typically found in megaraptorid and abelisauridtheropods. These results suggest a greater diversity of theropods in the original ecosystem than previously thought, including the presence of a second morphotype of megaraptorid and alvarezsaurid previously undocumented in this formation. Furthermore, the existence of Morphotype 6 indicates the potential coexistence of medium-sized abelisauroids alongside larger abelisaurids in the same ecosystem. These findings underscore the importance of future expeditions to the Sierra del Portezuelo locality to further our understanding of these previously unknown theropod species.
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... Acquisition was done with a PCO edge 4,2 sCMOS (PCO, Kelheim Germany), recording 10,000 projections for BP/1/4593 and 11,000 projections for BP/1/3895 and NMQR 389, with a total exposure time of 30 ms, with three accumulated images of 10 ms (Cau et al., 2017). The specimens were scanned with a 'tetra-acquisition' setup, with the centre of rotation shifted twice to create four radiographs that were stitched together in post processing to create a larger slice to encompass the complete specimen. ...
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Early Cretaceous Troodontine Troodontid (Dinosauria: Theropoda) from the Ohyamashimo Formation of Japan Reveals the Early Evolution of Troodontinae
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Full-text available
  • Jun 2024
A new troodontid dinosaur, Hypnovenator sasayamaensis gen. et sp. nov., is described based on an articulated postcranial skeleton recovered from the fluvial deposits of the Albian Ohyamashimo Formation of the Sasayama Group in Tambasasayama City, Hyogo Prefecture, Japan. Hypnovenator is distinguished from other troodontids by four autapomorphies and a combination of additional features. Our phylogenetic analysis positions Hypnovenator as the oldest and one of the most basal troodontines, forming a monophyletic clade with Gobivenator mongoliensis. The discovery of Hypnovenator suggests that small-bodied maniraptorans with a sleeping posture were common not only in environments with volcanic and eolian events or alluvial systems but also in fluvial systems. Geometric morphometric analysis of manual unguals shows that manual unguals I and III of Hypnovenator exhibit considerable morphological variation but are functionally similar, which differs from those of non-troodontine troodontids, reflecting the transition of manual motion within Troodontinae. Hypnovenator also has mosaic features in the pes related to cursoriality. This study reveals that asymmetrical arctometatarsus occurred by the Albian, and some morphological changes, such as shorter digit IV than digit III and non-ungual phalanges of digits III with roller joints and digit IV with weakly ginglymoid articulation, arose during the early Late Cretaceous.
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Pelvic and hindlimb muscular reconstruction of the paravian theropod Buitreraptor gonzalezorum and its palaeobiological implications
Article
  • Jan 2024
Soft tissue reconstructions of fossil vertebrates provide valuable data and support for functional interpretations. Here, we present the pelvic and hindlimb muscular reconstruction of Buitreraptor gonzalezorum, a unenlagiine dromaeosaurid theropod. Dromaeosaurids employed their hindlimbs for locomotion and predation, with a specialised pedal digit II. Using the ‘extant phylogenetic bracket’ methodology, we reconstruct 29 muscles out of the 37 typically found in extant archosaur hindlimbs. Some characteristics resemble those of specialised cursorial tetrapods. For example, M. iliotibialis shows an increased hip abduction moment arm, while primary protractors exhibit an increased hip flexion moment arm, and main retractors display a decreased hip extension moment arm. However, positive allometric growth of limb inertia relative to body mass and the gradual transition to a ‘knee-based’ locomotion observed in extant birds may have influenced muscle moment arms. Regarding predatory functions, the muscular features and length proportions of the metatarsus and pedal digit II phalanges suggest faster movements compared to derived dromaeosaurids. Also, a robust flexor muscle, likely M. flexor perforans et perforatus digiti II, was inserted on the proximoventral heel of the second phalanx of pedal digit II. These functional interpretations suggest the presence of specialised behaviours different from those observed in more derived dromaeosaurids.
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Complex neuroanatomy in the rostrum of the Isle of Wight theropod Neovenator salerii
Article
Full-text available
  • Jun 2017
The discovery of large, complex, internal canals within the rostra of fossil reptiles has been linked with an enhanced tactile function utilised in an aquatic context, so far in pliosaurids, the Cretaceous theropod Spinosaurus, and the related spinosaurid Baryonyx. Here, we report the presence of a complex network of large, laterally situated, anastomosing channels, discovered via micro-focus computed tomography (μCT), in the premaxilla and maxilla of Neovenator, a mid-sized allosauroid theropod from the Early Cretaceous of the UK. We identify these channels as neurovascular canals, that include parts of the trigeminal nerve; many branches of this complex terminate on the external surfaces of the premaxilla and maxilla where they are associated with foramina. Neovenator is universally regarded as a ‘typical’ terrestrial, predatory theropod, and there are no indications that it was aquatic, amphibious, or unusual with respect to the ecology or behaviour predicted for allosauroids. Accordingly, we propose that enlarged neurovascular facial canals shouldn’t be used to exclusively support a model of aquatic foraging in theropods and argue instead that an enhanced degree of facial sensitivity may have been linked with any number of alternative behavioural adaptations, among them defleshing behaviour, nest selection/maintenance or social interaction.
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Exceptionally prolonged tooth formation in elasmosaurid plesiosaurians
Article
Full-text available
Elasmosaurid plesiosaurians were globally prolific marine reptiles that dominated the Mesozoic seas for over 70 million years. Their iconic body-plan incorporated an exceedingly long neck and small skull equipped with prominent intermeshing ‘fangs’. How this bizarre dental apparatus was employed in feeding is uncertain, but fossilized gut contents indicate a diverse diet of small pelagic vertebrates, cephalopods and epifaunal benthos. Here we report the first plesiosaurian tooth formation rates as a mechanism for servicing the functional dentition. Multiple dentine thin sections were taken through isolated elasmosaurid teeth from the Upper Cretaceous of Sweden. These specimens revealed an average of 950 daily incremental lines of von Ebner, and infer a remarkably protracted tooth formation cycle of about 2–3 years–other polyphyodont amniotes normally take ~1–2 years to form their teeth. Such delayed odontogenesis might reflect differences in crown length and function within an originally uneven tooth array. Indeed, slower replacement periodicity has been found to distinguish larger caniniform teeth in macrophagous pliosaurid plesiosaurians. However, the archetypal sauropterygian dental replacement system likely also imposed constraints via segregation of the developing tooth germs within discrete bony crypts; these partly resorbed to allow maturation of the replacement teeth within the primary alveoli after displacement of the functional crowns. Prolonged dental formation has otherwise been linked to tooth robustness and adaption for vigorous food processing. Conversely, elasmosaurids possessed narrow crowns with an elongate profile that denotes structural fragility. Their apparent predilection for easily subdued prey could thus have minimized this potential for damage, and was perhaps coupled with selective feeding strategies that ecologically optimized elasmosaurids towards more delicate middle trophic level aquatic predation.
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The phylogenetic affinities of the bizarre Late Cretaceous Romanian theropod Balaur bondoc (Dinosauria, Maniraptora): Dromaeosaurid or flightless bird?
Article
Full-text available
  • Jun 2015
The exceptionally well-preserved Romanian dinosaur Balaur bondoc is the most complete theropod known to date from the Upper Cretaceous of Europe. Previous studies of this remarkable taxon have included its phylogenetic interpretation as an aberrant dromaeosaurid with velociraptorine affinities. However, Balaur displays a combination of both apparently plesiomorphic and derived bird-like characters. Here, we analyse those features in a phylogenetic revision and show how they challenge its referral to Dromaeosauridae. Our reanalysis of two distinct phylogenetic datasets focusing on basal paravian taxa supports the reinterpretation of Balaur as an avialan more crownward than Archaeopteryx but outside of Pygostylia, and as a flightless taxon within a paraphyletic assemblage of long-tailed birds. Our placement of Balaur within Avialae is not biased by character weighting. The placement among dromaeosaurids resulted in a suboptimal alternative that cannot be rejected based on the data to hand. Interpreted as a dromaeosaurid, Balaur has been assumed to be hypercarnivorous and predatory, exhibiting a peculiar morphology influenced by island endemism. However, a dromaeosaurid-like ecology is contradicted by several details of Balaur’s morphology, including the loss of a third functional manual digit, the non-ginglymoid distal end of metatarsal II, and a non-falciform ungual on the second pedal digit that lacks a prominent flexor tubercle. Conversely, an omnivorous ecology is better supported by Balaur’s morphology and is consistent with its phylogenetic placement within Avialae. Our reinterpretation of Balaur implies that a superficially dromaeosaurid-like taxon represents the enlarged, terrestrialised descendant of smaller and probably volant ancestors.
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A bizarre Jurassic maniraptoran theropod with preserved evidence of membranous wings
Article
Full-text available
  • Apr 2015
  • NATURE
The wings of birds and their closest theropod relatives share a uniform fundamental architecture, with pinnate flight feathers as the key component. Here we report a new scansoriopterygid theropod, Yi qi gen. et sp. nov., based on a new specimen from the Middle-Upper Jurassic period Tiaojishan Formation of Hebei Province, China. Yi is nested phylogenetically among winged theropods but has large stiff filamentous feathers of an unusual type on both the forelimb and hindlimb. However, the filamentous feathers of Yi resemble pinnate feathers in bearing morphologically diverse melanosomes. Most surprisingly, Yi has a long rod-like bone extending from each wrist, and patches of membranous tissue preserved between the rod-like bones and the manual digits. Analogous features are unknown in any dinosaur but occur in various flying and gliding tetrapods, suggesting the intriguing possibility that Yi had membranous aerodynamic surfaces totally different from the archetypal feathered wings of birds and their closest relatives. Documentation of the unique forelimbs of Yi greatly increases the morphological disparity known to exist among dinosaurs, and highlights the extraordinary breadth and richness of the evolutionary experimentation that took place close to the origin of birds.
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A Review of Dromaeosaurid Systematics and Paravian Phylogeny
Article
Full-text available
  • Aug 2012
Coelurosauria is the most diverse clade of theropod dinosaurs. Much of this diversity is present in Paraves—the clade of dinosaurs containing dromaeosaurids, troodontids, and avialans. Paraves has over 160 million years of evolutionary history that continues to the present day. The clade represents the most diverse living tetrapod group (there are over 9000 extant species of Aves—a word used here as synonomous with “bird”), and it is at the root of the paravian radiation, when dromaeosaurids, troodontids, and avialans were diverging from one another, that we find the morphology and soft tissue changes associated with the origin of modern avian flight. Within the first 15 million years of known paravian evolutionary history members of this clade exhibited a difference of nearly four orders of magnitude in body size, a value that is similar to the extreme body size disparity present today in mammalian carnivorans, avians, and varanoid squamates. In this respect, Paraves is an important case study in characterizing the patterns, processes, and dynamics of evolutionary size change. This last point is of particular interest because of the historical significance placed on the role of body size reduction in the origin of powered avian flight.Our study reviews and revises the membership of Dromaeosauridae and provides an apomorphy-based diagnosis for all valid taxa. Of the currently 31 named dromaeosaurid species, we found 26 to be valid. We provide the most detailed and comprehensive phylogenetic analysis of paravians to date in order to explore the phylogenetic history of dromaeosaurid taxa. The general pattern of paravian relationships is explored within the broader context of Coelurosauria with an emphasis on sampling basal avialans, because of their importance for character optimizations at the base of Paraves.A large dataset was constructed by merging two datasets, one examining coelurosaur relationships broadly (based on previous TWiG datasets) and the other examining avialan relationships specifically (Clarke et al., 2006). This merged dataset was then significantly revised and supplemented with novel character analysis focusing on paravian taxa. During character analysis, particular attention was given to basal members of Dromaeosauridae, enigmatic basal paravians such as Jinfengopteryx elegans and Anchiornis huxleyi, and the incorporation of new morphological information from two undescribed troodontid species from the Late Cretaceous of Mongolia. A final dataset of 474 characters scored for 111 taxa was used to address paravian evolution. This dataset is important in that it bridges a phylogenetic gap that had persisted between studies on birds and studies on all other coelurosaurs. Most scorings in this matrix were based on the direct observation of specimens.All most parsimonious trees recovered in the cladistic analysis support the monophyly of Paraves, Troodontidae, Dromaeosauridae, and Deinonychosauria. A new clade of basal troodontids is discovered including two undescribed Mongolian troodontids and Jinfengopteryx elegans. Xiaotingia and Anchiornis form a clade at the base of Troodontidae. Recently proposed relationships within Dromaeosauridae are further supported and a succession of clades from Gondwana and Asia form sister taxa to a clade of Laurasian dromaeosaurids. Avialan monophyly is strongly supported with Archaeopteryx, Sapeornis, Jeholornis, and Jixiangornis forming the successive sister taxa to the Confuciusornis node. This topology supports a more basal position for Sapeornis than previous phylogenetic analyses and indicates a progressive acquisition of a fully “avian” shoulder morphology.
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LOCOMOTOR MODULES AND THE EVOLUTION OF AVIAN FLIGHT
Article
  • Feb 1996
  • EVOLUTION
The evolution of avian flight can be interpreted by analyzing the sequence of modifications of the primitive tetrapod locomotor system through time. Herein, we introduce the term "locomotor module" to identify anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion. The first tetrapods, which employed lateral undulations of the entire body and appendages, had one large locomotor module. Basal dinosaurs and theropods were bipedal and possessed a smaller locomotor module consisting of the hind limb and tail. Bird flight evolved as the superimposition of a second (aerial) locomotor capability onto the ancestral (terrestrial) theropod body plan. Although the origin of the wing module was the primary innovation, alterations in the terrestrial system were also significant. We propose that the primitive theropod locomotor module was functionally and anatomically subdivided into separate pelvic and caudal locomotor modules. This decoupling freed the tail to attain a new and intimate affiliation with the forelimb during flight, a configuration unique to birds. Thus, the evolution of flight can be viewed as the origin and novel association of locomotor modules. Differential elaboration of these modules in various lineages has produced the diverse locomotor abilities of modern birds.
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How do cormorants counter buoyancy during submerged swimming?
Article
  • May 2004
Buoyancy is a de-stabilizing force for diving cormorants that forage at shallow depths. Having to counter this force increases the cost of transport underwater. Cormorants are known to be less buoyant than most water birds but are still highly buoyant (ρ=∼0.8 kg m–3) due to their adaptations for aerial flight. Nevertheless, cormorants are known to dive at a wide range of depths, including shallow dives where buoyancy is maximal. We analyzed the kinematics of underwater swimming of the great cormorant (Phalacrocorax carbo sinensis) in a shallow pool to discover and evaluate the mechanisms countering buoyancy while swimming horizontally. The birds maintained a very uniform cyclic paddling pattern. Throughout this cycle, synchronized tilting of the body, controlled by the tail, resulted in only slight vertical drifts of the center of mass around the average swimming path. We suggest that this tilting behavior serves two purposes: (1) the elongated bodies and the long tails of cormorants, tilted at a negative angle of attack relative to the swimming direction, generate downward directed hydrodynamic lift to resist buoyancy and (2) during the propulsive phase, the motion of the feet has a significant vertical component, generating a vertical component of thrust downward, which further helps to offset buoyancy. The added cost of the drag resulting from this tilting behavior may be reduced by the fact that the birds use a burst-and-glide pattern while swimming.
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Locomotor Modules and the Evolution of Avian Flight
Article
  • Feb 1996
The evolution of avian flight can be interpreted by analyzing the sequence of modifications of the primitive tetrapod locomotor system through time. Herein, we introduce the term "locomotor module" to identify anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion. The first tetrapods, which employed lateral undulations of the entire body and appendages, had one large locomotor module. Basal dinosaurs and theropods were bipedal and possessed a smaller locomotor module consisting of the hind limb and tail. Bird flight evolved as the superimposition of a second (aerial) locomotor capability onto the ancestral (terrestrial) theropod body plan. Although the origin of the wing module was the primary innovation, alterations in the terrestrial system were also significant. We propose that the primitive theropod locomotor module was functionally and anatomically subdivided into separate pelvic and caudal locomotor modules. This decoupling freed the tail to attain a new and intimate affiliation with the forelimb during flight, a configuration unique to birds. Thus, the evolution of flight can be viewed as the origin and novel association of locomotor modules. Differential elaboration of these modules in various lineages has produced the diverse locomotor abilities of modern birds.
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