Advertisement

The Skull and Head Muscles of Archosauria

  • Daniel Smith-ParedesEmail author
  • Bhart-Anjan S. Bhullar
Chapter
First Online:
Part of the Fascinating Life Sciences book series (FLS)

Abstract

Archosaurs is the clade composed by birds (Aves) and crocodiles, alligators, and the gharial (Crocodylia). This relatedness is not obvious and for a long time was not taken into account, as birds were seen as a group separate even from the rest of reptiles. Both avians and crocodylians are morphologically very distinct and in many aspects different from each other and from the ancestral forms within Archosauria. The skulls of birds are composed of thin and light bones, many fused to each other, and others articulating in mobile joints allowing the beak to move and bend with respect to the rest of the skull. In crocodylians the skulls are massive and heavy, a solid akinetic structure built to crush prey. The accompanying muscle system, attaching onto and responsible for the movement of the head, jaws, eyes, or tongue, is equally distinct. As a result of the striking differences and the relatively recent realization of crocodylians and avians being closely related, the comparison of their anatomy has never been very straightforward. This chapter’s goal is to provide a review of archosaur anatomy and to give at least some sense of the similarities and differences between archosaur musculature.

Keywords

Archosauria Aves Crocodylia Neognathae Palaeognathae Skull Jaw Tongue Hyoid Nostril musculature Orbitotemporal musculature Auricular musculature Temporal and palatal musculature Jaw and tongue musculature Neck musculature 
This is a preview of subscription content, log in to check access.

References

  1. Barsbold R, Osmolska H (1990) Ornithomimosauria. In: The Dinosauria. University of California Press, Berkeley, pp 225–244Google Scholar
  2. Barsbold R, Maryanska T, Osmolska H (1990) Oviraptorosauria. In: The Dinosauria, vol 1. University of California Press, Berkeley, pp 249–258Google Scholar
  3. Baumel JJ, King AS, Breazile JE, Evans HE, Vanden Berge JC (1993) Handbook of avian anatomy: nomina anatomica avium. Publications of the Nuttall Ornithological Club, CambridgeGoogle Scholar
  4. Bellairs AdA, Kamal A (1981) The chondrocranium and the development of the skull in recent reptiles. Biol Reptilia 11:1–264Google Scholar
  5. Bellairs AD, Shute CC (1953) Observations on the narial musculature of Crocodilia and its innervation from the sympathetic system. J Anat 87:367PubMedPubMedCentralGoogle Scholar
  6. Benton MJ, Clark JM (1988) Archosaur phylogeny and the relationships of the Crocodylia. In: The phylogeny and classification of the tetrapods, vol 1. Clarendon Press, Oxford, pp 295–338Google Scholar
  7. Berv JS, Field DJ (2017) Genomic signature of an avian Lilliput effect across the K-Pg extinction. Syst Biol 67(1):1–13PubMedCentralCrossRefPubMedGoogle Scholar
  8. Bhullar BA, Marugan-Lobon J, Racimo F et al (2012) Birds have paedomorphic dinosaur skulls. Nature 487:223–226PubMedCrossRefGoogle Scholar
  9. Brusatte SL, Benton MJ, Desojo JB, Langer MC (2010) The higher-level phylogeny of Archosauria (Tetrapoda: Diapsida). J Syst Palaeontol 8(1):3–47Google Scholar
  10. Burke AC, Nowicki JL (2003) A new view of patterning domains in the vertebrate mesoderm. Dev Cell 4:159–165PubMedCrossRefGoogle Scholar
  11. Chamberlain FW (1943) Atlas of avian anatomy; osteology, arthrology, myology. Michigan State College, Agricultural Experiment Station, East LansingGoogle Scholar
  12. Chiappe LM, Norell MA, Clark JM (1998) The skull of a relative of the stem-group bird Mononykus. Nature 392:275–278CrossRefGoogle Scholar
  13. Cleuren J, De Vree F (2000) Feeding in crocodilians. In: Feeding: form, function, and evolution in tetrapod vertebrates. Academic Press, New York, pp 337–358CrossRefGoogle Scholar
  14. Dal Sasso C, Signore M (1998) Exceptional soft-tissue preservation in a theropod dinosaur from Italy. Nature 392:383–387CrossRefGoogle Scholar
  15. Dalla Vecchia FM (2013) Triassic pterosaurs. Geol Soc Lond, Spec Publ 379:119–155CrossRefGoogle Scholar
  16. Desojo JB, Heckert AB, Martz JW et al (2013) Aetosauria: a clade of armoured pseudosuchians from the Upper Triassic continental beds. Geol Soc Lond, Spec Publ 379:203–239CrossRefGoogle Scholar
  17. Dilkes DW, Hutchinson JR, Holliday CM, Witmer LM (2012) Reconstructing the musculature of dinosaurs. In: The complete dinosaur. Indiana University Press, Bloomington, pp 151–190Google Scholar
  18. Elzanowski A (1987) Cranial and eyelid muscles and ligaments of the tinamous. Zoologische Jahrbücher (Abteilung für Anatomie) 116:63–118Google Scholar
  19. Evans DJ, Noden DM (2006) Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev Dyn 235:1310–1325PubMedCrossRefGoogle Scholar
  20. Evans DC, Reisz RR, Dupuis K (2007) A juvenile Parasaurolophus (Ornithischia: Hadrosauridae) braincase from Dinosaur Provincial Park, Alberta, with comments on crest ontogeny in the genus. J Vertebr Paleontol 27:642–650CrossRefGoogle Scholar
  21. Ezcurra MD, Butler RJ, Gower DJ (2013) ‘Proterosuchia’: the origin and early history of Archosauriformes. Geol Soc Lond, Spec Publ 379:9–33CrossRefGoogle Scholar
  22. Fabbri M, Koch NM, Pritchard AC et al (2017) The skull roof tracks the brain during the evolution and development of reptiles including birds. Nat Ecol Evol 1(10):1543PubMedCrossRefGoogle Scholar
  23. Fanti F, Currie PJ, Badamgarav D (2012) New specimens of Nemegtomaia from the Baruungoyot and Nemegt formations (Late Cretaceous) of Mongolia. PLoS One 7:e31330PubMedPubMedCentralCrossRefGoogle Scholar
  24. Fitzgerald, T.C. (1969). The coturnix quail: anatomy and histology. The coturnix quail: anatomy and histology.Google Scholar
  25. Gauthier J (1986) Saurischian monophyly and the origin of birds. In: Memoirs of the California Academy of Sciences, vol 8. University of California, Berkeley, pp 1–55Google Scholar
  26. Gauthier J, Kluge AG, Rowe T (1988) Amniote phylogeny and the importance of fossils. Cladistics 4:105–209CrossRefGoogle Scholar
  27. Gauthier JA, Nesbitt SJ, Schachner ER, Bever GS, Joyce WG (2011) The bipedal stem crocodilian Poposaurus gracilis: inferring function in fossils and innovation in archosaur locomotion. BullPeabody Mus Nat Hist 52:107–126CrossRefGoogle Scholar
  28. George JC, Berger AJ (1966) Avian myology. Academic Press, New YorkGoogle Scholar
  29. Grigg GC (2015) Biology and evolution of crocodylians. CSIRO, CollingwoodGoogle Scholar
  30. Holliday CM (2009) New insights into dinosaur jaw muscle anatomy. Anat Rec 292:1246–1265CrossRefGoogle Scholar
  31. Holliday CM, Witmer LM (2007) Archosaur adductor chamber evolution: integration of musculoskeletal and topological criteria in jaw muscle homology. J Morphol 268:457–484PubMedCrossRefGoogle Scholar
  32. Holliday CM, Witmer LM (2009) The epipterygoid of crocodyliforms and its significance for the evolution of the orbitotemporal region of eusuchians. J Vertebr Paleontol 29:715–733CrossRefGoogle Scholar
  33. Homberger DG, Meyers RA (1989) Morphology of the lingual apparatus of the domestic chicken, Gallus gallus, with special attention to the structure of the fasciae. Dev Dyn 186:217–257Google Scholar
  34. Horner JR, Weishampel DB, Forster C (2004) Hadrosauridae. In: The dinosauria, vol 2. University of California Press, Berkeley, pp 438–463CrossRefGoogle Scholar
  35. Iordansky NN (1973) The skull of the crocodilia. In: Biology of the reptilia, vol 4. Academic Press, London, pp 201–262Google Scholar
  36. Irmis RB, Nesbitt SJ, Sues H (2013) Early crocodylomorpha. Geol Soc Lond, Spec Publ 379:275–302CrossRefGoogle Scholar
  37. Jarvis ED, Mirarab S, Aberer AJ et al (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–1331PubMedPubMedCentralCrossRefGoogle Scholar
  38. Kardong KV (2006) Vertebrates: comparative anatomy, function, evolution. McGraw-Hill, New YorkGoogle Scholar
  39. King AS (1993) Apparatus respiratorius (systema respiratorium). In: Handbook of avian anatomy: nomina anatomica avium. Nuttall Ornithological Club, Cambridge, pp 257–299Google Scholar
  40. Kingsley JS (1912) Comparative anatomy of vertebrates, 1912. P. Blakiston’s, Philadelphia [591.4]Google Scholar
  41. Klembara J (2004) Ontogeny of the palatoquadrate and adjacent lateral cranial wall of the endocranium in prehatching Alligator mississippiensis (Archosauria: Crocodylia). J Morphol 262:644–658PubMedCrossRefGoogle Scholar
  42. Kulesa P, Ellies DL, Trainor PA (2004) Comparative analysis of neural crest cell death, migration, and function during vertebrate embryogenesis. Dev Dyn 229:14–29PubMedCrossRefGoogle Scholar
  43. Kundrát M (2008) HNK-1 immunoreactivity during early morphogenesis of the head region in a nonmodel vertebrate, crocodile embryo. Naturwissenschaften 95:1063PubMedCrossRefGoogle Scholar
  44. Kundrát M (2009) Heterochronic shift between early organogenesis and migration of cephalic neural crest cells in two divergent evolutionary phenotypes of archosaurs: crocodile and ostrich. Evol Dev 11:535–546PubMedCrossRefGoogle Scholar
  45. Le Lièvre CS (1978) Participation of neural crest-derived cells in the genesis of the skull in birds. Development 47:17–37Google Scholar
  46. Le Lièvre CS, Le Douarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. Development 34:125–154Google Scholar
  47. Li Z (2015) Evolution of the hyoid apparatus in Archosauria: implications for the origin of avian tongue function. The University of Texas, AustinGoogle Scholar
  48. Li Z, Clarke JA (2015) New insight into the anatomy of the hyolingual apparatus of Alligator mississippiensis and implications for reconstructing feeding in extinct archosaurs. J Anat 227:45–61PubMedPubMedCentralCrossRefGoogle Scholar
  49. Liyong J, Jun C, Shuqin Z, Butler RJ, Godefroit P (2010) Cranial anatomy of the small ornithischian dinosaur Changchunsaurus parvus from the Quantou formation (Cretaceous: Aptian-Cenomanian) of Jilin Province, northeastern China. J Vertebr Paleontol 30:196–214CrossRefGoogle Scholar
  50. Luther A (1914) Über die vom n. Trigeminus versorgte Muskulatur der Amphhibien. Druckerei der Finnischen Literaturgesellschaft, HelsingforsGoogle Scholar
  51. Madsen JH Jr (1976) Allosaurus fragilis: a revised osteology. Utah Geol Min Survey Bull 109:1–163Google Scholar
  52. Marpmann JS, Carballido JL, Sander PM, Knötschke N (2015) Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri (Dinosauria, Camarasauromorpha): ontogenetic changes and size dimorphism. J Syst Palaeontol 13:221–263CrossRefGoogle Scholar
  53. McIntosh JS (1990) Sauropoda. In: The dinosauria, vol 1. University of California Press, Berkeley, pp 345–401Google Scholar
  54. Nesbitt SJ (2011) The early evolution of archosaurs: relationships and the origin of major clades. Bull Am Mus Nat Hist 352:1–292CrossRefGoogle Scholar
  55. Nesbitt SJ, Desojo JB, Irmis RB (2013) Anatomy, phylogeny and palaeobiology of early archosaurs and their kin. Geol Soc Lond, Spec Publ 379:1–7CrossRefGoogle Scholar
  56. Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218PubMedCrossRefPubMedCentralGoogle Scholar
  57. Noden DM, Marcucio R, Borycki AG, Emerson CP (1999) Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis. Dev Dyn 216:96–112PubMedCrossRefGoogle Scholar
  58. Ősi A (2005) Hungarosaurus tormai, a new ankylosaur (Dinosauria) from the Upper Cretaceous of Hungary. J Vertebr Paleontol 25:370–383CrossRefGoogle Scholar
  59. Ostrom JH (1976) Archaeopteryx and the origin of birds. Biol J Linn Soc 8:91–182CrossRefGoogle Scholar
  60. Parker WK (1866) On the structure and development of the skull in the ostrich tribe. Philos Trans R Soc Lond 156:113–183CrossRefGoogle Scholar
  61. Pérez-Moreno P, Sanz JL, Buscalioni AD et al (1994) A unique multitoothed ornithomimosaur dinosaur from the lower cretaceous of Spain. Nature 370:363–367CrossRefGoogle Scholar
  62. Prum RO (1992) Syringeal morphology, phylogeny, and evolution of the neotropical manakins (Aves, Pipridae). American Museum novitates; no. 3043Google Scholar
  63. Prum RO, Berv JS, Dornburg A et al (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–573PubMedCrossRefGoogle Scholar
  64. Pycraft WP (1900) On the morphology and phylogeny of the Palæognathæ (Ratitæand Crypturi) and Neognathæ (Carinatæ). J Zool 15:149–290Google Scholar
  65. Rieppel O (2000) Turtles as diapsid reptiles. Zool Scr 29:199–212CrossRefGoogle Scholar
  66. Romer AS (1956) Osteology of the reptiles. University of Chicago Press, ChicagoGoogle Scholar
  67. Santagati F, Rijli FM (2003) Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 4:806–818PubMedCrossRefGoogle Scholar
  68. Schumacher GH (1973) The head muscles and hyolaryngeal skeleton of turtles and crocodilians. In: Biology of the reptilia, vol 4. Academic Press, London, pp 101–200Google Scholar
  69. Schwab IR, Brooks DE (2002) He cries crocodile tears…. Br J Ophthalmol 86:23–23PubMedPubMedCentralCrossRefGoogle Scholar
  70. Sereno PC, Shichin C, Zhengwu C, Chenggang R (1988) Psittacosaurus meileyingensis (Ornithischia: Ceratopsia), a new psittacosaur from the Lower Cretaceous of northeastern China. J Vertebr Paleontol 8:366–377CrossRefGoogle Scholar
  71. Shih HP, Gross MK, Kioussi C (2008) Muscle development: forming the head and trunk muscles. Acta Histochem 110:97–108PubMedCrossRefGoogle Scholar
  72. Shute CCD, Bellairs A (1955) The external ear in crocodilia. J Zool 124:741–749Google Scholar
  73. Stocker MR, Butler RJ (2013) Phytosauria. Geol Soc Lond, Spec Publ 379:91–117CrossRefGoogle Scholar
  74. Sues H-D, Galton PM (1987) Anatomy and classification of the North American Pachycephalosauria (Dinosauria: Ornithischia). E. Schweizerbart’sche, StuttgartGoogle Scholar
  75. Tomlinson B (2000) Feeding in paleognathous birds. In: Feeding: form, function, and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 359–394CrossRefGoogle Scholar
  76. Tsai HP, Holliday CM (2011) Ontogeny of the alligator cartilago transiliens and its significance for sauropsid jaw muscle evolution. PLoS One 6:e24935PubMedPubMedCentralCrossRefGoogle Scholar
  77. Tsuihiji T (2005) Homologies of the transversospinalis muscles in the anterior presacral region of Sauria (crown Diapsida). J Morphol 263:151–178PubMedCrossRefGoogle Scholar
  78. Tsuihiji T (2007) Homologies of the longissimus, iliocostalis, and hypaxial muscles in the anterior presacral region of extant Diapsida. J Morphol 268:986–1020PubMedCrossRefGoogle Scholar
  79. Tsuihiji T (2010) Reconstructions of the axial muscle insertions in the occipital region of dinosaurs: evaluations of past hypotheses on Marginocephalia and Tyrannosauridae using the extant phylogenetic bracket approach. Anat Rec 293:1360–1386CrossRefGoogle Scholar
  80. Underwood G (1970) The eye. In: Biology of the reptilia, vol 2. Academic Press, London, pp 1–97Google Scholar
  81. Unwin DM (2003) On the phylogeny and evolutionary history of pterosaurs. Geol Soc Lond Spec Publ 217:139–190CrossRefGoogle Scholar
  82. Van den Berge C, Zweers GA (1993) Myologia. In: Handbook of avian anatomy: nomina anatomica avium. Nuttall Ornithological Club, Cambridge, pp 189–247Google Scholar
  83. Vickaryous MK (2006) New information on the cranial anatomy of Edmontonia rugosidens Gilmore, a late cretaceous nodosaurid dinosaur from Dinosaur Provincial Park, Alberta. J Vertebr Paleontol 26:1011–1013CrossRefGoogle Scholar
  84. Vullo R, Marugán-Lobón J, Kellner A et al (2012) A new crested pterosaur from the early cretaceous of Spain: the first European tapejarid (Pterodactyloidea: Azhdarchoidea). PLoS One 7:e38900PubMedPubMedCentralCrossRefGoogle Scholar
  85. Wang X, Kellner A, Zhou Z, de Almeida Campos D (2007) A new pterosaur (Ctenochasmatidae, Archaeopterodactyloidea) from the lower Cretaceous Yixian Formation of China. Cretac Res 28:245–260CrossRefGoogle Scholar
  86. Wang X, Kellner AW, Jiang S, Cheng X (2012) New toothed flying reptile from Asia: close similarities between early cretaceous pterosaur faunas from China and Brazil. Naturwissenschaften 99:249–257PubMedCrossRefGoogle Scholar
  87. Wang S, Stiegler J, Amiot R et al (2017a) Extreme ontogenetic changes in a ceratosaurian theropod. Curr Biol 27:144–148PubMedCrossRefGoogle Scholar
  88. Wang S, Stiegler J, Wu P et al (2017b) Heterochronic truncation of odontogenesis in theropod dinosaurs provides insight into the macroevolution of avian beaks. Proc Natl Acad Sci U S A 114(41):10930–10935PubMedPubMedCentralCrossRefGoogle Scholar
  89. Webb M (1957) The ontogeny of the cranial bones, cranial peripheral and cranial parasympathetic nerves, together with a study of the visceral muscles of Struthio. Acta Zool 38:81–203CrossRefGoogle Scholar
  90. Wedin B (1953) The development of the eye muscles in Ardea cinerea L. Cells Tissues Organs 18:30–48CrossRefGoogle Scholar
  91. Weishampel DB, Witmer LM (1990) Heterodontosauridae. In: The dinosauria, vol 1. University of California Press, Berkeley, pp 486–497Google Scholar
  92. Whitlock JA (2011) A phylogenetic analysis of Diplodocoidea (Saurischia: Sauropoda). Zool J Linn Soc 161:872–915CrossRefGoogle Scholar
  93. Winokur RM (1982) Erectile tissue and smooth muscle in snouts of Carettochelys insculpta, trionchids and other chelonia. Zoomorphology 101:83–93CrossRefGoogle Scholar
  94. Witmer LM (1995) Homology of facial structures in extant archosaurs (birds and crocodilians), with special reference to paranasal pneumaticity and nasal conchae. J Morphol 225:269–327PubMedCrossRefGoogle Scholar
  95. Witmer LM (1997) The evolution of the antorbital cavity of archosaurs: a study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. J Vertebr Paleontol 17:1–76CrossRefGoogle Scholar
  96. Witmer LM, Chatterjee S, Franzosa J, Rowe T (2003) Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425:950PubMedCrossRefGoogle Scholar
  97. Zusi RL (1993) Patterns of diversity in the avian skull. The Skull 2:391–437Google Scholar
  98. Zusi R, Livezey B (2000) Homology and phylogenetic implications of some enigmatic cranial features in galliform and anseriform birds. Ann Carnegie Mus 69:157–193Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Geology and GeophysicsYale UniversityNew HavenUSA

Personalised recommendations

Cite chapter

Buy options