Journal of Mammalian Evolution

, Volume 20, Issue 4, pp 291–307 | Cite as

Digital Reconstruction of the Otic Region and Inner Ear of the Non-Mammalian Cynodont Brasilitherium riograndensis (Late Triassic, Brazil) and Its Relevance to the Evolution of the Mammalian Ear

  • Pablo Gusmão RodriguesEmail author
  • Irina Ruf
  • Cesar Leandro Schultz
Original Paper


The external anatomy of the petrosal, the bony labyrinth of the inner ear, and the stapes of Brasilitherium riograndensis (specimen UFRGS-PV-1043-T) were investigated by digital 3D reconstructions based on μCT scan images. Brasilitherium is the most basal taxon bearing a distinct promontorium, although less inflated than that of Morganucodon and still lacking a flat medial facet. A bony wall formed by the petrosal separates the cochlear canal and the vestibule from the brain cavity, with an internal acoustic meatus bearing distinct foramina for the facial nerve (VII) and vestibulocochlear nerve (VIII). The semicircular canals are irregular in shape, the anterior canal being the largest and the lateral one the smallest. Brasilitherium has an elongated but straight cochlear canal. The stapes resembles the morphology of derived non-mammaliaform cynodonts, such as Probainognathus and Pachygenelus, and differs from Thrinaxodon. By the allometric relationship of the cochlear canal and the estimated body mass, Brasilitherium can be grouped with Yunnanodon and Morganucodon in a regression line, which is below the line of mammals and above the line of non-avian reptiles. Brasilitherium fits in a sequence of gradual elongation of the cochlear canal associated with the enhancement in the capacity to hear higher frequencies. Among the constraints that might have triggered these transformations in small, insectivorous, and possibly nocturnal Mesozoic cynodont taxa is the improvement of detecting acoustically active insects.


Inner ear evolution Brasilitherium Cynodonts μCT scan Triassic 



We thank José Fernando Bonaparte, Wolfgang Maier, Zhe-Xi Luo, John R. Wible, Téo Veiga de Oliveira, Marina Bento Soares, Daniel Fortier, and Alessandra Boos. Irmgard Pfeifer-Schäller made the μCT scan.


  1. Abdala F (2007) Redescription of Platycraniellus elegans (Therapsida, Cynodontia) from the Lower Triassic of South Africa, and the cladistic relationships of eutheriodonts. Palaeontology 50(3): 591–618CrossRefGoogle Scholar
  2. Allin EF (1975) Evolution of the mammalian middle ear. J Morphol 147: 403–438.CrossRefPubMedGoogle Scholar
  3. Allin EF (1986) The auditory apparatus of advanced mammal-like reptiles and early mammals. In: Hotton N III, Maclean PD, Roth JJ, Roth EC (eds) The Ecology and Biology of Mammal-like Reptiles. Smithsonian Institution Press, Washington, DC, pp 283–294Google Scholar
  4. Allin EF, Hopson JA (1992) Evolution of the auditory system in synapsida ("mammal-like reptiles" and primitive mammals) as seen in the fossil record. In: Popper AN, Webster DB, Fay RR (eds) The Evolutionary Biology of Hearing. Springer-Verlag, Berlin, pp. 587–614Google Scholar
  5. Blanks RHI, Curthoys IS, Bennett ML, Markham CH (1985) Planar relationships of the semicircular canals in rhesus and squirrel monkeys. Brain Res 340: 315–324CrossRefPubMedGoogle Scholar
  6. Blanks RHI, Estes MS, Markham CH (1975) Physiologic characteristics of vestibular first order canal neurons in cat. II. Response to constant angular acceleration. J Neurophysiol 38: 1250–1268PubMedGoogle Scholar
  7. Bonaparte JF, Martinelli AG, Schultz CL (2005) New information on Brasilodon and Brasilitherium (Cynodontia, Probainognathia) from the Late Triassic of southern Brazil. Rev Brasil Paleontol 8(1):25–46Google Scholar
  8. Bonaparte JF, Martinelli AG, Schultz CL, Rupert R (2003) The sister group of mammals: small cynodonts from the Late Triassic of southern Brazil. Rev Brasil Paleontol 5: 5–27Google Scholar
  9. Brink AS (1955) A study on the skeleton of Diademodon. Palaeontol Afr 3:3–39Google Scholar
  10. Calabrese DR, Hullar TE (2006) Planar relationships of the two semicircular canals in two strains of mice. J Assoc Res Otolaryngol 7: 151–159PubMedCentralCrossRefPubMedGoogle Scholar
  11. Cox CB (1962) A natural cast of the inner ear of a dicynodont. Am Mus Novitates 2116: 1–6Google Scholar
  12. Cox CB, Jeffery N (2010) Semicircular canals and agility: the influence of size and shape measures. J Anat 216: 37–47PubMedCentralCrossRefPubMedGoogle Scholar
  13. Crompton AW (1964) On the skull of Oligokyphus. Bull Brit Mus Nat Hist Geol 21: 27–71Google Scholar
  14. Cummins H (1925) The vestibular labyrinth of the albino rat: form and dimensions and the orientation of the semicircular canals, cristae and maculae. J Comp Neurol 38: 399–445CrossRefGoogle Scholar
  15. Curthoys IS, Blanks RHI, Markham CH (1977) Semicircular canal radii of curvature (R) in cat, guinea pig and man. J Morphol 151: 1–16CrossRefPubMedGoogle Scholar
  16. Ekdale EG, Rowe T (2011) Morphology and variation within the bony labyrinth of zhelestids (Mammalia, Eutheria) and other therian mammals. J Vertebr Paleontol 31:658–675CrossRefGoogle Scholar
  17. Estes R (1961) Cranial anatomy of the cynodont reptile Thrinaxodon liorhinus. Bull Mus Comp Zool 125: 165–180Google Scholar
  18. Fourie J (1974) The cranial morphology of Thrinaxodon liorhinus Seeley. Ann S Afr Mus 65: 337–400Google Scholar
  19. Fox RC, Meng J (1997) An X-radiograph and SEM study of the osseous inner ear of multituberculates and monotremes (Mammalia): implications for mammalian phylogeny and the evolution of hearing. Zool J Linn Soc 121: 249–291CrossRefGoogle Scholar
  20. Gingerich PD, Smith BH (1984) Allometric scaling in the dentition of primates and insectivores. In: Jungers WL (ed) Size and Scaling in Primate Biology. Plenum, New York, pp 257–272Google Scholar
  21. Gow CE (1985) Apomorphies of the Mammalia. S Afr Sci 81: 558–560Google Scholar
  22. Gow CE (1986) A new skull of Megazostrodon (Mammalia, Triconodonta) from the Elliot Formation (Lower Jurassic) of southern Africa. Palaeontol Afr 26:13–23Google Scholar
  23. Graybeal A, Rosowski JJ, Ketten DR, Crompton AW (1989) Inner-ear structure in Morganucodon, an Early Jurassic mammal. Zool J Linn Soc 96: 107–117CrossRefGoogle Scholar
  24. Gu J-J, Montealegre-Z F, Robert D, Engel MS, Qiao G-X, Ren D (2012) Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females. Proc Natl Acad Sci USA, doi  10.1073/pnas.1118372109
  25. Hopson JA (1964) The braincase of the advanced mammal-like reptile Bienotherium. Postilla 87: 1–30Google Scholar
  26. Hopson JA (1966) The origin of the mammalian middle ear. Am Zool 6: 437–450CrossRefPubMedGoogle Scholar
  27. Hopson JA, Barghusen H (1986) An analysis of therapsid relationships. In: Hotton N III, Maclean PD, Roth JJ, Roth EC (eds) The Ecology and Biology of Mammal-like Reptiles. Smithsonian Institution Press, Washington, DC, pp 83–106Google Scholar
  28. Hopson JA, Kitching JW (2001) A probainognathian cynodont from South Africa and the phylogeny of non-mammalian cynodonts. In: Jenkins FA Jr, Shapiro MD, Owerkowicz T (eds) Studies in Organismic and Evolutionary Biology in Honor of Alfred W. Crompton. Bull Mus Comp Zool 156: 5–35Google Scholar
  29. Hurum JH (1998) The inner ear of two Late Cretaceous multituberculate mammals, and its implications for multituberculate hearing. J Mammal Evol 5: 65–93CrossRefGoogle Scholar
  30. Kemp TS (1980) Aspects of the structure and functional anatomy of the Middle Triassic cynodont Luangwa. J Zool 191: 193–239Google Scholar
  31. Kermack KA, Mussett F, Rigney HW (1981) The skull of Morganucodon. Zool J Linn Soc 53: 87–175CrossRefGoogle Scholar
  32. Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the Age of Dinosaurs: Origin, Evolution, and Structure. Columbia University Press, New York, 630 ppGoogle Scholar
  33. Kühne WG (1956) The Liassic Therapsid Oligokyphus. Trustees of the British Museum (Natural History), London, 149 ppGoogle Scholar
  34. Ladevèze S, Muizon C de, Colbert M, Smith T (2010) 3D computational imaging of the petrosal of a new multituberculate mammal from the Late Cretaceous of China and its paleobiologic inferences. C R Palevol 9: 319–330Google Scholar
  35. Lillegraven JA, Hahn G (1993) Evolutionary analysis of the middle and inner ear of Late Jurassic multituberculates. J Mammal Evol 1: 47–74CrossRefGoogle Scholar
  36. Lillegraven JA, Krusat G (1991) Cranio-mandibular anatomy of Haldanodon exspectatus (Docodonta, Mammalia) from the Late Jurassic of Portugal and its implications to the evolution of mammalian characters. Contrib Geol Univ of Wyoming 28: 39–138Google Scholar
  37. Liu J, Olsen P (2010) The phylogenetic relationships of Eucynodontia (Amniota: Synapsida). J Mammal Evol 17:151–176.CrossRefGoogle Scholar
  38. Lucas SG, Luo Z-X (1993) Adelobasileus from the Upper Triassic of west Texas: the oldest mammal. J Vertebr Paleontol 13: 309–334CrossRefGoogle Scholar
  39. Luo Z-X (1994) Sister-group relationships of mammals and transformations of diagnostic mammalian characters In: Fraser NC, Sues HD (eds) In the Shadow of the Dinosaurs: Early Mesozoic Tetrapods. Cambridge University Press, New York, pp 98–128Google Scholar
  40. Luo Z–X (2001) Inner ear and its bony housing in tritylodonts and implications for evolution of mammalian ear. In: Jenkins FA Jr, Shapiro MD, Owerkowicz T (eds) Studies in Organismic and Evolutionary Biology in Honor of Alfred W. Crompton. Bull Mus Comp Zool 156: 81–97Google Scholar
  41. Luo Z-X (2007) Transformation and diversification in early mammal evolution. Nature 450: 1011–1019CrossRefPubMedGoogle Scholar
  42. Luo Z-X (2011) Developmental patterns in Mesozoic evolution of mammal ears. Annu Rev Ecol Evol Syst 42: 355–380.CrossRefGoogle Scholar
  43. Luo Z-X, Crompton AW (1994) Transformation of quadrate (incus) through the transition from non-mammalian cynodonts to mammals. J Vertebr Paleontol 14: 341–374CrossRefGoogle Scholar
  44. Luo Z-X, Crompton AW, Lucas SG (1995) Evolutionary origins of the mammalian promontorium and cochlea. J Vertebr Paleontol 15: 113–121CrossRefGoogle Scholar
  45. Luo Z-X, Crompton AW, Sun A-L (2001) A new mammaliaform from the Early Jurassic and evolution of mammalian characteristics. Science 292:1535–1540Google Scholar
  46. Luo Z-X, Ketten DR (1991) CT scanning and computerized reconstructions of the inner ear structure of multituberculate mammals. J Vertebr Paleontol 11: 220–228Google Scholar
  47. Luo Z-X, Kielan-Jaworowska Z, Cifelli RL (2002) In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol Pol 47:1–78Google Scholar
  48. Luo Z-X, Ruf I, Martin T (2012) The petrosal and inner ear of the Late Jurassic cladotherian mammal Dryolestes leiriensis and implications for evolution of ear in therian mammals. Zool J Linn Soc 166:433–463.CrossRefGoogle Scholar
  49. Luo Z-X, Ruf I, Schultz JA, Martin T (2011) Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. Proc R Soc B 278: 28–34PubMedCentralCrossRefPubMedGoogle Scholar
  50. Luo Z-X, Wible JR (2005) A Late Jurassic digging mammal and early mammalian diversity. Science 308:103–107CrossRefPubMedGoogle Scholar
  51. Manley GA (1971) Some aspects of the evolution of hearing in vertebrates. Nature 230: 506–509CrossRefPubMedGoogle Scholar
  52. Manley GA (1973) A review of some currents concepts of the functional evolution of the ear. Evolution 26: 608–621CrossRefGoogle Scholar
  53. Martinez RN, May CL, Forster CA (1996) A new carnivorous cynodont from the Ischigualasto Formation (Late Triassic, Argentina), with comments on eucynodont phylogeny. J Vertebr Paleontol 16(2): 271–284CrossRefGoogle Scholar
  54. Matano S, Kubo T, Matsunaga T, Niemitz C, Günther M, Taub DM, King FA (1986) Current Perspectives in Primate Biology. Van Nostrand Reinhold, New YorkGoogle Scholar
  55. Meng J, Wyss AR (1995) Monotreme affinities and low-frequency hearing suggested by multituberculate ear. Nature 377: 141–144CrossRefGoogle Scholar
  56. Miao D (1988) Skull morphology of Lambdopsalis bulla (Mammalia, Multituberculata) and its implications to mammalian evolution. Contrib Geol Univ Wyoming 4: 1–104Google Scholar
  57. Novacek MJ, Wyss AR (1986) Origin and transformation of the mammalian stapes. Contrib Geol Univ Wyoming Spec Pap 3:35–53Google Scholar
  58. Olson EC (1944) Origin of mammals based upon the cranial-morphology of therapsid suborders. Geol Soc Am Spec Paper 55: 1–136CrossRefGoogle Scholar
  59. Quiroga JC (1979) The inner ear of two cynodonts (Reptilia—Therapsida) and some comments on the evolution of the inner ear from pelycosaurs to mammals. Gegenbaurs Morphol Jb 125: 178–190Google Scholar
  60. Ramprashad F, Landolt JP, Money KE, Laufer J (1980) Neuromorphometric features and dimensional analysis of the vestibular end organ in the little brown bat (Myotis lucifugus). J Comp Neurol 192: 883–902CrossRefPubMedGoogle Scholar
  61. Romer AS (1970) The Chañares (Argentina) Triassic reptile fauna. VI. A chiniquodontid cynodont with an incipient squamosal-dentary jaw articulation. Breviora 344: 1–18Google Scholar
  62. Rosowski JJ, Graybeal A (1991) What did Morganucodon hear? Zool J Linn Soc 101: 131–168CrossRefGoogle Scholar
  63. Rougier GW, Wible JR, Hopson JA (1992) Reconstruction of the cranial vessels in the Early Cretaceous mammal Vincelestes neuquenianus: implications for the evolution of mammalian cranial vascular system. J Vertebr Paleontol 12: 188–216Google Scholar
  64. Rougier GW, Wible JR, Hopson JA (1996) Basicranial anatomy of Priacodon fruitaensis (Triconodontidae, Mammalia) from the Late Jurassic of Colorado, and a reappraisal of mammaliaform interrelationships. Am Mus Novitates 3183: 1–38.Google Scholar
  65. Rowe T (1988) Definition, diagnosis and origin of Mammalia. J Vertebr Paleontol 8(3): 241–264CrossRefGoogle Scholar
  66. Rowe T, Carlson W, Bottorff W (1993) Thrinaxodon, Digital Atlas of the Skull, CD-ROM. University of Texas Press, AustinGoogle Scholar
  67. Ruf I, Luo Z-X, Martin T (in press) Re-investigation of the basicranium of Haldanodon exspectatus (Docodonta, Mammaliaformes). J Vertebr PaleontolGoogle Scholar
  68. Ruf I, Luo Z-X, Wible JR, Martin T (2009) Petrosal anatomy and inner ear structures of the Late Jurassic Henkelotherium (Mammalia, Cladotheria, Dryolestoidea): insight into the early evolution of the ear region in cladotherian mammals. J Anat 214: 679–693PubMedCentralCrossRefPubMedGoogle Scholar
  69. Sigogneau D (1974) The inner ear of Gorgonops (Reptilia, Therapsida, Gorgonospsia). Ann S Afr Mus 64: 53–69Google Scholar
  70. Spoor F, Garland T Jr, Krovitz G, Ryan TM, Silcox MT, Walker A (2007) The primate semicircular canal system and locomotion. Proc Natl Acad Sci USA 104 (26): 10808–10812PubMedCentralCrossRefPubMedGoogle Scholar
  71. Spoor F, Zonneveld F (1995) Morphometry of the primate bony labyrinth: a new method based on high-resolution computed tomography. J Anat 186:271–86PubMedCentralPubMedGoogle Scholar
  72. Sues H-D (1986) The skull and dentition of two tritylodontid synapsids from the Lower Jurassic of western North America. Bull Mus Comp Zool 151: 217–268Google Scholar
  73. Sun A-L (1984) Skull morphology of the tritylodontid genus Bienotheroides of Sichuan. Sci Sinica Ser B 27: 270–284Google Scholar
  74. Sun A-L, Cui G-H (1987) Otic region in tritylodont Yunnanodon. Vertebr PalAsia 25: 1–7Google Scholar
  75. Wible JR (1991) Origin of Mammalia: the craniodental evidence reexamined. J Vertebr Paleontol 11: 1–28CrossRefGoogle Scholar
  76. Wible JR, Hopson JA (1993) Basicranial evidence for early mammal phylogeny. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Early Therians, and Marsupials. Sringer-Verlag, New York, pp 45–62CrossRefGoogle Scholar
  77. Williams PL, Williams R, Dyson M, Bannister LH (1989) Gray’s Anatomy, 37th edition. Churchill Livingstone, New York, 1,598 ppGoogle Scholar
  78. Zeller U (1989) The braincase of Ornithorhynchus. Fortschr Zool 35:386–391Google Scholar
  79. Zerfass H, Lavina EL, Schultz CL, Garcia AJV, Faccini UF, Chemale F Jr (2003) Sequence-stratigraphy of continental strata of southernmost Brazil: a contribution to Southwestern Gondwana palaeogeography and palaeoclimate. Sedimentary Geol 161: 85–105CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Pablo Gusmão Rodrigues
    • 1
    Email author
  • Irina Ruf
    • 2
  • Cesar Leandro Schultz
    • 1
  1. 1.Laboratório de Paleovertebrados, Departamento de Paleontologia e Estratigrafia, Instituto de GeociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Steinmann-Institut für Geologie, Mineralogie und PaläontologieRheinische Friedrich-Wilhelms-Universität BonnBonnGermany

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