The neuroanatomy and pneumaticity of Hamadasuchus (Crocodylomorpha, Peirosauridae) from the Cretaceous of Morocco and its paleoecological significance for altirostral forms

We describe the endocranial structures of Hamadasuchus, a peirosaurid crocodylomorph from the late Albian-Cenomanian Kem Kem group of Morocco. The cranial endocast, associated nerves and arteries, endosseous labyrinths, and cranial pneumatization, as well as the bones of the braincase of a new specimen, are reconstructed and compared with extant and fossil crocodylomorphs, which represent different lifestyles. Cranial bones of this specimen are identified as belonging to Hamadasuchus, with close affinities with Rukwasuchus yajabalijekundu, another peirosaurid from the 'middle' Cretaceous of Tanzania. The endocranial structures are comparable to those of R. yajabalijekundu but also to baurusuchids and sebecids (sebecosuchians). Paleobiological traits of Hamadasuchus, such as alert head posture, ecology, and behavior are explored for the first time, using quantitative metrics. The expanded but narrow semi-circular canals and enlarged pneumatization of the skull of Hamadasuchus are linked to a terrestrial lifestyle. Continuing work on the neuroanatomy of supposedly terrestrial crocodylomorphs needs to be broadened to other groups and will allow to characterize whether some internal structures are affected by the lifestyle of these organisms.

[1]  P. Mannion,et al.  Neuroanatomy of the crocodylian Tomistoma dowsoni from the Miocene of North Africa provides insights into the evolutionary history of gavialoids , 2023, Journal of anatomy.

[2]  J. Martin,et al.  A peirosaurid mandible from the Albian–Cenomanian (Lower Cretaceous) of Algeria and the taxonomic content of Hamadasuchus (Crocodylomorpha, Peirosauridae) , 2023, Papers in Palaeontology.

[3]  O. Mateus,et al.  Neuroanatomy of the crocodylomorph Portugalosuchus azenhae from the late cretaceous of Portugal , 2023, Journal of anatomy.

[4]  J. Lachambre,et al.  Ontogenetic variability of the intertympanic sinus distinguishes lineages within Crocodylia , 2023, Journal of anatomy.

[5]  J. Cubo,et al.  A survey of osteoderm histology and ornamentation among Crocodylomorpha: A new proxy to infer lifestyle? , 2022, Journal of morphology.

[6]  Jorgo Ristevski.  Neuroanatomy of the mekosuchine crocodylian Trilophosuchus rackhami Willis, 1993 , 2022, Journal of anatomy.

[7]  Pedro L. Godoy,et al.  Body size estimation of Caimaninae specimens from the miocene of South America , 2022, Journal of South American Earth Sciences.

[8]  R. Elsey,et al.  Ontogeny of the trigeminal system and associated structures in Alligator mississippiensis , 2022, Journal of morphology.

[9]  James M. Clark,et al.  Anatomy and relationships of the early diverging Crocodylomorphs Junggarsuchus sloani and Dibothrosuchus elaphros , 2022, Anatomical record.

[10]  J. Canudo,et al.  New data on the neuroanatomy of basal eusuchian crocodylomorphs (Allodaposuchidae) from the Upper Cretaceous of Spain , 2022, Cretaceous Research.

[11]  S. Walsh,et al.  Ontogenetic variation in the crocodylian vestibular system , 2021, Journal of anatomy.

[12]  J. Adrien,et al.  The neuroanatomy of Zulmasuchus querejazus (Crocodylomorpha, Sebecidae) and its implications for the paleoecology of sebecosuchians , 2021, Anatomical record.

[13]  A. Turner,et al.  Reevaluation of the cranial osteology and phylogenetic position of the early crocodyliform Eopneumatosuchus colberti, with an emphasis on its endocranial anatomy , 2021, Anatomical record.

[14]  P. Mannion,et al.  A second peirosaurid crocodyliform from the Mid-Cretaceous Kem Kem Group of Morocco and the diversity of Gondwanan notosuchians outside South America , 2021, Royal Society Open Science.

[15]  S. Pierce,et al.  Cranial and endocranial anatomy of a three‐dimensionally preserved teleosauroid thalattosuchian skull , 2021, Anatomical record.

[16]  S. Morozov,et al.  Braincase anatomy of extant Crocodylia, with new insights into the development and evolution of the neurocranium in crocodylomorphs , 2021, Journal of anatomy.

[17]  A. Turner,et al.  Braincase anatomy of the Paleocene crocodyliform Rhabdognathus revealed through high resolution computed tomography , 2021, PeerJ.

[18]  K. N. Dollman,et al.  Deep evolutionary diversification of semicircular canals in archosaurs , 2021, Current Biology.

[19]  M. Bronzati,et al.  A new species of Caipirasuchus (Notosuchia, Sphagesauridae) from the Late Cretaceous of Brazil and the evolutionary history of Sphagesauria , 2021 .

[20]  S. Walsh,et al.  The Braincase and Inner Ear of ‘Metriorhynchus’ cf. ‘M.’ Brachyrhynchus – Implications for Aquatic Sensory Adaptations in Crocodylomorphs , 2021, Journal of Vertebrate Paleontology.

[21]  E. Rayfield,et al.  Ontogenetic endocranial shape change in alligators and ostriches and implications for the development of the non-avian dinosaur endocranium. , 2020, Anatomical record.

[22]  R. M. Santucci,et al.  Paleoneurology of Baurusuchus (Crocodyliformes: Baurusuchidae), ontogenetic variation, brain size, and sensorial implications , 2020, Anatomical record.

[23]  C. Holliday,et al.  A 3D ontogenetic atlas of Alligator mississippiensis cranial nerves and their significance for comparative neurology of reptiles , 2020, Anatomical record.

[24]  A. Iwaniuk,et al.  Endocast structures are reliable proxies for the sizes of corresponding regions of the brain in extant birds , 2020, Journal of anatomy.

[25]  D. Martill,et al.  Geology and paleontology of the Upper Cretaceous Kem Kem Group of eastern Morocco , 2020, ZooKeys.

[26]  James M. Clark,et al.  Inner ear sensory system changes as extinct crocodylomorphs transitioned from land to water , 2020, Proceedings of the National Academy of Sciences.

[27]  James M. Clark,et al.  Braincase anatomy of Almadasuchus figarii (Archosauria, Crocodylomorpha) and a review of the cranial pneumaticity in the origins of Crocodylomorpha , 2020, Journal of anatomy.

[28]  C. Schultz,et al.  Morphology of the endocranial cavities of Campinasuchus dinizi (Crocodyliformes: Baurusuchidae) from the Upper Cretaceous of Brazil , 2020 .

[29]  S. Lautenschlager,et al.  Neuroanatomical and neurosensorial analysis of the Late Cretaceous basal eusuchian Agaresuchus fontisensis (Cuenca, Spain) , 2020, Papers in Palaeontology.

[30]  M. Norell,et al.  The bony labyrinth of Platecarpus (Squamata: Mosasauria) and aquatic adaptations in squamate reptiles , 2019 .

[31]  Ariana Paulina-Carabajal,et al.  Novel information on the endocranial morphology of the abelisaurid theropod Carnotaurus sastrei , 2019, Comptes Rendus Palevol.

[32]  M. Lamanna,et al.  A New Peirosaurid Crocodyliform from the Upper Cretaceous Lago Colhué Huapi Formation of Central Patagonia, Argentina , 2019, Annals of Carnegie Museum.

[33]  P. Currie,et al.  A new and complete peirosaurid (Crocodyliformes, Notosuchia) from Sierra Barrosa (Santonian, Upper Cretaceous) of the Neuquén Basin, Argentina , 2019, Cretaceous Research.

[34]  Fabien Knoll,et al.  Brain and pneumatic cavities of the braincase of the basal alligatoroid Diplocynodon tormis (Eocene, Spain) , 2019, Journal of Vertebrate Paleontology.

[35]  S. Lautenschlager,et al.  Inner skull cavities of the basal eusuchian Lohuecosuchus megadontos (Upper Cretaceous, Spain) and neurosensorial implications , 2019, Cretaceous Research.

[36]  M. Norell,et al.  Are endocasts good proxies for brain size and shape in archosaurs throughout ontogeny? , 2018, Journal of anatomy.

[37]  Y. Herrera,et al.  Braincase and endocranial anatomy of two thalattosuchian crocodylomorphs and their relevance in understanding their adaptations to the marine environment , 2018, PeerJ.

[38]  J. Sayão,et al.  Bone microanatomy of Pepesuchus deiseae (Mesoeucrocodylia, Peirosauridae) reveals a mature individual from the Upper Cretaceous of Brazil , 2018, Cretaceous Research.

[39]  Z. Gasparini,et al.  New Patagonian baurusuchids (Crocodylomorpha; Notosuchia) from the Bajo de la Carpa Formation (Upper Cretaceous; Neuquén, Argentina): New evidences of the early sebecosuchian diversification in Gondwana , 2018, Comptes Rendus Palevol.

[40]  A. Martinelli,et al.  The first Caipirasuchus (Mesoeucrocodylia, Notosuchia) from the Late Cretaceous of Minas Gerais, Brazil: new insights on sphagesaurid anatomy and taxonomy , 2018, PeerJ.

[41]  J. Desojo,et al.  Paleoneuroanatomy of the aetosaur Neoaetosauroides engaeus (Archosauria: Pseudosuchia) and its paleobiological implications among archosauriforms , 2018, PeerJ.

[42]  R. Bertini,et al.  New material ofPepesuchus(Crocodyliformes; Mesoeucrocodylia) from the Bauru Group: implications about its phylogeny and the age of the Adamantina Formation , 2018, Zoological Journal of the Linnean Society.

[43]  K. Angielczyk,et al.  The Braincase and Endocast of Parringtonia gracilis, a Middle Triassic Suchian (Archosauria: Pseudosuchia) , 2017, Journal of Vertebrate Paleontology.

[44]  A. Garrido,et al.  A new peirosaurid from the Bajo de la Carpa Formation (Upper Cretaceous, Santonian) of Cerro Overo, Neuquén, Argentina , 2017 .

[45]  Ariana Paulina-Carabajal,et al.  Neuroanatomy of the abelisaurid theropod Viavenator: The most complete reconstruction of a cranial endocast and inner ear for a South American representative of the clade , 2017 .

[46]  J. Janáček,et al.  Volume of the crocodilian brain and endocast during ontogeny , 2017, PloS one.

[47]  S. Pierce,et al.  Virtual reconstruction of the endocranial anatomy of the early Jurassic marine crocodylomorph Pelagosaurus typus (Thalattosuchia) , 2017, PeerJ.

[48]  S. Walsh,et al.  The Braincase and Neurosensory Anatomy of an Early Jurassic Marine Crocodylomorph: Implications for Crocodylian Sinus Evolution and Sensory Transitions , 2016, Anatomical record.

[49]  L. Witmer,et al.  Vascular patterns in the heads of crocodilians: blood vessels and sites of thermal exchange , 2016, Journal of anatomy.

[50]  J. Martin,et al.  A Miniature Notosuchian with Multicuspid Teeth from the Cretaceous of Morocco , 2016, Journal of Vertebrate Paleontology.

[51]  H. Larsson,et al.  Revision and phylogenetic affinities of Elosuchus (Crocodyliformes) , 2016 .

[52]  F. Agnolin,et al.  A new peirosaurid (Crocodilyformes) from the Late Cretaceous (Turonian–Coniacian) of Patagonia, Argentina , 2016 .

[53]  Pedro L. Godoy,et al.  Postcranial anatomy of Pissarrachampsa sera (Crocodyliformes, Baurusuchidae) from the Late Cretaceous of Brazil: insights on lifestyle and phylogenetic significance , 2016, PeerJ.

[54]  H. Larsson,et al.  The evolution of the meatal chamber in crocodyliforms , 2016, Journal of anatomy.

[55]  D. Pol,et al.  A new Late Cretaceous crocodyliform from the western margin of Gondwana (La Rioja Province, Argentina) , 2016 .

[56]  D. Pol,et al.  The Postcranial Anatomy of Yacarerani boliviensis and the Phylogenetic Significance of the Notosuchian Postcranial Skeleton , 2015 .

[57]  L. Witmer,et al.  Ontogeny of the Middle-Ear Air-Sinus System in Alligator mississippiensis (Archosauria: Crocodylia) , 2015, PloS one.

[58]  I. S. Carvalho,et al.  Osteoderms of Montealtosuchus arrudacamposi (Crocodyliformes, Peirosauridae) from the Turonian-Santonian (Upper Cretaceous) of Bauru Basin, Brazil , 2015 .

[59]  J. Fortuny,et al.  Distributed under Creative Commons Cc-by 4.0 a New Species of Allodaposuchus (eusuchia, Crocodylia) from the Maastrichtian (late Cretaceous) of Spain: Phylogenetic and Paleobiological Implications , 2022 .

[60]  L. Xing,et al.  Braincase Anatomy of the Basal Theropod Sinosaurus from the Early Jurassic of China , 2014 .

[61]  P. O’Connor,et al.  A New Crocodyliform from the Middle Cretaceous Galula Formation, Southwestern Tanzania , 2014 .

[62]  D. Pol,et al.  A New Notosuchian from the Late Cretaceous of Brazil and the Phylogeny of Advanced Notosuchians , 2014, PloS one.

[63]  A. Kellner,et al.  A New Sebecid from the Paleogene of Brazil and the Crocodyliform Radiation after the K–Pg Boundary , 2014, PloS one.

[64]  Paula Bona,et al.  Caiman gasparinae sp. nov., a huge alligatorid (Caimaninae) from the late Miocene of Paraná, Argentina , 2013 .

[65]  Z. Gasparini.  LOS NOTOSUCHIA DEL CRETACICO DE AMERICA DEL SUR COMO UN NUEVO INFRAORDEN DE LOS MESOSUCHIA (CROCODILIA). , 2013 .

[66]  L. Chiappe,et al.  The variability of inner ear orientation in saurischian dinosaurs: testing the use of semicircular canals as a reference system for comparative anatomy , 2013, PeerJ.

[67]  T. Marinho,et al.  Gondwanasuchus scabrosus gen. et sp. nov., a new terrestrial predatory crocodyliform (Mesoeucrocodylia: Baurusuchidae) from the Late Cretaceous Bauru Basin of Brazil , 2013 .

[68]  C. Holliday,et al.  Trigeminal Nerve Morphology in Alligator mississippiensis and Its Significance for Crocodyliform Facial Sensation and Evolution , 2013, Anatomical record.

[69]  Paula Bona,et al.  Skull Anatomy of the Bizarre Crocodylian Mourasuchus nativus (Alligatoridae, Caimaninae) , 2013, Anatomical record.

[70]  Ariana Paulina-Carabajal,et al.  The Endocranial Morphology and Inner Ear of the Abelisaurid Theropod Aucasaurus garridoi , 2013 .

[71]  M. Krause,et al.  Postcranial Anatomy of Sebecus icaeorhinus (Crocodyliformes, Sebecidae) from the Eocene of Patagonia , 2012 .

[72]  C. Holliday,et al.  A New Eusuchian Crocodyliform with Novel Cranial Integument and Its Significance for the Origin and Evolution of Crocodylia , 2012, PloS one.

[73]  D. Pol,et al.  A new sebecid mesoeucrocodylian from the Rio Loro Formation (Palaeocene) of north-western Argentina , 2011 .

[74]  H. Zaher,et al.  The skull of the Upper Cretaceous baurusuchid crocodile Baurusuchus albertoi Nascimento & Zaher 2010, and its phylogenetic affinities , 2011 .

[75]  Z. Gasparini,et al.  A Metriorhynchid Crocodyliform Braincase from Northern Chile , 2011 .

[76]  A. Turner,et al.  Craniofacial Morphology of Simosuchus clarki (Crocodyliformes: Notosuchia) from the Late Cretaceous of Madagascar , 2010 .

[77]  A. Turner,et al.  Phylogenetic History of Simosuchus clarki (Crocodyliformes: Notosuchia) from the Late Cretaceous of Madagascar , 2010 .

[78]  H. Larsson,et al.  Cretaceous Crocodyliforms from the Sahara , 2009 .

[79]  D. Pol,et al.  The first crocodyliform from the Chubut Group (Chubut Province, Argentina) and its phylogenetic position within basal Mesoeucrocodylia , 2009 .

[80]  L. Witmer,et al.  New Insights Into the Brain, Braincase, and Ear Region of Tyrannosaurs (Dinosauria, Theropoda), with Implications for Sensory Organization and Behavior , 2009, Anatomical record.

[81]  Michael P Taylor,et al.  Head and Neck Posture in Sauropod Dinosaurs Inferred from Extant Animals , 2009 .

[82]  L. Witmer,et al.  The Paranasal Air Sinuses of Predatory and Armored Dinosaurs (Archosauria: Theropoda and Ankylosauria) and Their Contribution to Cephalic Structure , 2008, Anatomical record.

[83]  Paul C. Sereno,et al.  Structural Extremes in a Cretaceous Dinosaur , 2007, PloS one.

[84]  H. Larsson,et al.  Cranial osteology and phylogenetic relationships of Hamadasuchus rebouli (Crocodyliformes: Mesoeucrocodylia) from the Cretaceous of Morocco , 2007 .

[85]  I. S. Carvalho,et al.  CONDICIONANTE ETOLÓGICO NA TAFONOMIA DE UBERABASUCHUS TERRIFICUS (CROCODYLIFORMES, PEIROSAURIDAE) DA BACIA BAURU (CRETÁCEO SUPERIOR) , 2007 .

[86]  T. Hullar.  Semicircular canal geometry, afferent sensitivity, and animal behavior. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[87]  A. Turner.  Osteology and phylogeny of a new species of Araripesuchus (Crocodyliformes: Mesoeucrocodylia) from the Late Cretaceous of Madagascar , 2006 .

[88]  J. Klembara,et al.  Ontogeny of the partial secondary wall of the otoccipital region of the endocranium in prehatching Alligator mississippiensis (Archosauria, Crocodylia) , 2005, Journal of morphology.

[89]  Á. Buscalioni,et al.  A NEW SPECIES OF DORATODON (CROCODYLIFORMES: ZIPHOSUCHIA) FROM THE LATE CRETACEOUS OF SPAIN , 2005 .

[90]  M. Norell,et al.  A New Crocodyliform from Zos Canyon, Mongolia , 2004 .

[91]  Sankar Chatterjee,et al.  Neuroanatomy of flying reptiles and implications for flight, posture and behaviour , 2003, Nature.

[92]  H. Larsson,et al.  A NEW NOTOSUCHIAN FROM THE EARLY CRETACEOUS OF NIGER , 2003 .

[93]  H. Larsson,et al.  A new Early Cretaceous crocodyliform from Niger , 2000 .

[94]  Paul M. Magwene,et al.  Predatory Dinosaurs from the Sahara and Late Cretaceous Faunal Differentiation , 1996, Science.

[95]  J. Parrish.  Phylogeny of the Crocodylotarsi, with reference to archosaurian and crurotarsan monophyly , 1993 .

[96]  A. D. Walker.  A Revision of Sphenosuchus acutus Haughton, a Crocodylomorph Reptile from the Elliot Formation (Late Triassic or Early Jurassic) of South Africa , 1990 .

[97]  A. Busbey.  New material of Sebecus cf. huilensis (Crocodilia: Sebecosuchidae) from the Miocene La Venta Formation of Colombia , 1986 .

[98]  J. Hopson.  Relative Brain Size and Behavior in Archosaurian Reptiles , 1977 .

[99]  E. H. Colbert.  The Eustachian Tubes in the Crocodilia , 1946 .

[100]  David K. Smith,et al.  The endocranium of the theropod dinosaur Ceratosaurus studied with computed tomography , 2005 .

[101]  E. Buffetaut.  A new crocodilian from the Cretaceous of southern Morocco , 1994 .

[102]  S. J. Phillips,et al.  Head orientation in pigeons: postural, locomotor and visual determinants. , 1989, Brain, behavior and evolution.

[103]  A. Hudspeth.  The Hair Cells of the Inner Ear , 1983 .

[104]  G. Simpson,et al.  Sebecus, representative of a peculiar suborder of fossil Crocodilia from Patagonia. Bulletin of the AMNH ; v. 87, article 4 , 1946 .