Journal of Mammalian Evolution

, Volume 5, Issue 1, pp 65–93 | Cite as

The Inner Ear of Two Late Cretaceous Multituberculate Mammals, and Its Implications for Multituberculate Hearing

  • Jørn H. Hurum


The inner ear of the Late Cretaceous multituberculates Nemegtbaatar gobiensis and Chulsan-baatar vulgaris is described from serial sections and enlarged models. The size and proportions of the inner ear as a whole are as expected for extant small mammals. The lengths of the cochlea (Nemegtbaatar gobiensis, 3.0 mm, Chulsanbaatar vulgaris, 2.0 mm) are comparable to those of other multituberculates, when ratios of length of the cochlea to skull length are calculated. The vestibule is not as expanded in the two taxa as in Lambdopsalis, ?Meniscoessus, and ?Catopsalis; the estimated volume for Nemegtbaatar gobiensis is 9 mm3. A slightly laterally curved, anteriomedially directed cochlea, relatively robust ear ossicles, and the estimations of the area of the tympanic membrane and stapedial footplate in Chulsanbaatar suggest high-frequency hearing but a relatively low sensitivity to low-decibel sounds. The semicircular canals of Nemegtbaatar and Chulsanbaatar are fully developed; the size of the anterior, posterior, and lateral canals and their angles and proportions are comparable to those of extant mammals of similar size. The anterior semicircular canal of Nemegtbaatar forms a smooth half-circle and thus is more derived than the angular canal of Ornithorhynchus. The notable differences between the ratio of the width of the lateral semicircular canal to skull length and the size of the vestibule in Nemegtbaatar and the Paleocene multituberculate Lambdopsalis bulla are probably related to different modes of life.

Multituberculata inner ear cochlea semicircular canals hearing evolution 


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  1. Allin, E. F. (1986). The auditory apparatus of advanced mammal-like reptiles and early mammals. In: The Ecology and Biology of Mammal-like Reptiles, N. Hotton, P. M. Maclean, J. J. Roth, and E. C. Koth, eds., pp. 283–294, Smithsonian University Press, Washington, DC.Google Scholar
  2. Allin, E. F., and Hopson, J. A. (1992). Evolution of the auditory system in Synapsida (“mammal-like reptiles” and primitive mammals) as seen in the fossil record. In: The Evolutionary Biology of Hearing, D. B. Webster, R. R. Fay, and A. N. Popper, eds., pp. 587–614, Springer-Verlag, New York.Google Scholar
  3. Averianov, A. O. (1997). New Late Cretaceous mammals of southern Khazakhstan. Acta Palaeontol. Polonica 46: 243–256.Google Scholar
  4. Blanks, R. H. I., Estes, M. S., and Markham, C. H. (1975). Physiologic characteristics of vestibular first-order canal neurons in the cat. II. Response to constant angular acceleration. J. Neurophysiol. 38: 1250–1268.Google Scholar
  5. Broom, R. (1914). On the structure and affinities of the Multituberculata. Bull. Am. Mus. Nat. Hist. 33: 115–134.Google Scholar
  6. Crompton, A. W. (1963). Tooth replacement in the cynodont Thrinaxodon liorhinus Seeley. Ann. S. Afr. Mus. 44: 479–521.Google Scholar
  7. Curthoys, I. S., Blanks, R. H. I., and Markham, C. H. (1977). Semicircular canal radii of curvature (R) in cat, guinea pig and man. J. Morphol. 151: 1–16.Google Scholar
  8. Eisenberg, J. F. (1981). The Mammalian Radiations: An Analysis of the Trends in Evolution, Adaption, and Behavior, University of Chicago Press, Chicago.Google Scholar
  9. Estes, R. (1961). Cranial anatomy of the cynodont reptile Thrinaxodon liorhinus. Bull. Mus. Comp. Zool. 125: 165–180.Google Scholar
  10. Evans, H. E., and Christensen, G. C. (1979). Miller's Anatomy of the Dog, W. B. Saunders, Philadelphia.Google Scholar
  11. Fernandez, C., and Schmidt, R. S. (1963). The opossum ear and the evolution of the coiled cochlea. J. Comp. Neurol. 121: 151–159.Google Scholar
  12. Fourie, S. (1974). The cranial morphology of Thrinaxodon liorhinus Seeley. Ann. S. Afr. Mus. 65: 337–400.Google Scholar
  13. Fox, R. C., and 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: 249–291.Google Scholar
  14. Grassé, P. P. (1967). Traité de Zoologie, Anatomie, Systématique, Biologie, Tome XVI, Frasicule 1. Mammifères: Téguments et Squelette, Masson, Paris.Google Scholar
  15. Gray, A. A. (1907). The Labyrinth of Animals, Vols. 1 and 2, J. and A. Churchill, London.Google Scholar
  16. Gray, O. (1951). An introduction to the study of the comparative anatomy of the labyrinth. J. Laryngol. Otol. 65: 681–703.Google Scholar
  17. Gray, O. (1955). A brief survey of the phylogenesis of the labyrinth. J. Laryngol. Otol. 69: 151–178.Google Scholar
  18. Graybeal, A., Rosowski, J. J., Ketten, D. R., and Crompton, A. W. (1989). Inner-ear structure in Morganucodon, an early Jurassic mammal. Zool. J. Linn. Soc. 96: 107–117.Google Scholar
  19. Hopson, J. A. (1964). The braincase of the advanced mammal-like reptile Bienotherium. Postilla 87: 1–30.Google Scholar
  20. Hurum, J. H. (1994). The snout and orbit of Mongolian multituberculates studied by serial sections. Acta Palaeontol. Polonica 39: 181–224.Google Scholar
  21. Hurum, J. H. (1998). The braincase of two Late Cretaceous Asian multituberculates studied by serial sections. Acta Palaeontol. Polonica 43: 21–52.Google Scholar
  22. Hurum, J. H., Presley, R., and Kielan-Jaworowska, Z. (1996). The middle ear in multituberculate mammals. Acta Palaeontol. Polonica 41: 253–275.Google Scholar
  23. Jenkins, F. A., Jr., and Krause, D. W. (1983). Adaptations for climbing in North American multituberculates (Mammalia). Science 220: 713–715.Google Scholar
  24. Jerison, H. (1973). Evolution of Brain and Intelligence, Academic Press, New York.Google Scholar
  25. Jerzykiewicz, T., and Russell, D. A. (1991). Late Mesozoic stratigraphy and vertebrates of the Gobi Basin. Cretaceous Res. 12: 345–377.Google Scholar
  26. Kermack, K. A., and Mussett, F. (1983). The ear in mammal-like reptiles and early mammals. Acta Palaeontol. Polonica 28: 147–158.Google Scholar
  27. Kermack, K. A., Mussett, F., and Rigney, H. W. (1981). The skull of Morganucodon. Zool. J. Linn. Soc. 53: 87–175.Google Scholar
  28. Kielan-Jaworowska, Z. (1974). Multituberculate succession in the Late Cretaceous of the Gobi Desert (Mongolia). Paleontol. Polonica 30: 23–44.Google Scholar
  29. Kielan-Jaworowska, Z., and Gambaryan, P. P. (1994). Postcranial anatomy and habits of Asian multituberculate mammals. Fossils Strata 36: 1–92.Google Scholar
  30. Kielan-Jaworowska, Z., and Hurum, J. H. (1997). Djadochtatheria—a new suborder of multituberculate mammals. Acta Palaeontol. Polonica 42: 201–242.Google Scholar
  31. Kielan-Jaworowska, Z., and Qi, T. (1990). Fossorial adaptations of a taeniolabidoid multituberculate mammal from the Eocene of China. Vertebr. PalAs. 28: 81–94.Google Scholar
  32. Kielan-Jaworowska, Z., Poplin, C., Presley, R., and de Riqlès, A. (1984). Preliminary data on multituberculate cranial anatomy studied by serial sections. In: Third Symposium on Mesozoic Terrestrial Ecosystems, W. E. Reif and F. Westphal, eds., pp. 123–128, Attempto Verlag, Tübingen.Google Scholar
  33. Kielan-Jaworowska, Z., Presley, R. and Poplin, C. (1986). The cranial vascular system in taeniolabidoid multituberculate mammals. Phil. Trans. R. Soc. Lond. B 313: 525–602.Google Scholar
  34. Krause, D. W., and Kielan-Jaworowska, Z. (1993). The endocranial cast and encephalization quotient of Ptilodus (Multituberculata, Mammalia). Palaeovertebrata 22: 99–112.Google Scholar
  35. Lewis, R. E., Leverenz, E. L., and Bialek, W. S. (1985). The Vertebrate Inner Ear, CRC Press, Boca Raton, FL.Google Scholar
  36. Lillegraven, J. A., and Hahn, G. (1993). Evolutionary analysis of the middle and inner ear of Late Jurassic multituberculates. J. Mammal. Evol. 1: 47–74.Google Scholar
  37. Lillegraven, J. A., and Krusat, G. (1991). Cranio-mandibular anatomy of Haldanodon exspectatus (Docodonta; Mammalia) from the Late Jurassic of Portugal and its implication to the evolution of mammalian characters. Contr. Geol. Univ. Wyo. 28: 39–138.Google Scholar
  38. Luo, Z. (1989). Structure of the Petrosals of Multituberculata (Mammalia) and Morphology of the Molars of Early Arctocyonids (Condylarthra, Mammalia), Ph.D. dissertation, University of California, Berkeley.Google Scholar
  39. Luo, Z. (1994). Sister-group relationships of mammals and transformations of diagnostic mammalian characters. In: In the Shadow of the Dinosaurs—Early Mesozoic Tetrapods, N. C. Fraser and H.-D. Sues, eds., pp. 98–128, Cambridge University Press, Cambridge.Google Scholar
  40. Luo, Z., and Crompton, A. W. (1994). Transformation of the quadrate (incus) through the transition from non-mammalian cynodonts to mammals. J. Vertebr. Paleontol. 14: 341–374.Google Scholar
  41. Luo, Z. and Ketten, D. R. (1991). CT scanning and computerized reconstructions of the inner ear of multituberculate mammals. J. Vertebr. Paleontol. 11: 220–228.Google Scholar
  42. Luo, Z., Crompton, A. W., and Lucas, S. G. (1995). Evolutionary origins of the mammalian promontorium and cochlea. J. Vertebr. Paleontol. 15: 113–121.Google Scholar
  43. Manley, G. A. (1971). Some aspects of the evolution of hearing in vertebrates. Nature 230: 506–509.Google Scholar
  44. Matanao, S., Kubo, T., Matsunaga, T., Niemitz, C., and Gunther, M. (1986). On the semicircular canals organ in the Tarsius bancanus. In Current Perspectives in Primate Biology, M. B. Taub and F. A. King, eds., pp. 122–129, Van Nostrand Reinhold, New York.Google Scholar
  45. Meng, J. (1992). The stapes of Lambdopsalis bulla (Multituberculata) and transformational analysis of some stapedial features in Mammaliaformes. J. Vertebr. Paleontol. 12: 459–471.Google Scholar
  46. Meng, J., and Fox, R. C. (1993). Inner ear structures from Late Cretaceous mammals and their systematic and functional implications. J. Vertebr. Paleontol. 13(Suppl.): 50a.Google Scholar
  47. Meng, J., and Fox, R. C. (1995a). Evolution of the inner ear from non-therians during the Mesozoic: Implications for mammalian phylogeny and hearing. In: Sixth Symposium on Mesozoic Terrestrial Ecosystems and Biota, Short Papers, A. Sun and Y. Wang, eds., pp. 235–242, China Ocean Press, Beijing.Google Scholar
  48. Meng, J., and Fox, R. C. (1995b). Osseous inner ear structures and hearing in early marsupials and placentals. Zool. J. Linn. Soc. 115: 47–71.Google Scholar
  49. Meng, J., and Wyss, A. R. (1995). Monotreme affinities and low-frequency hearing suggested by multituberculate ear. Nature 377: 141–144.Google Scholar
  50. Miao, D. (1988). Skull morphology of Lambdopsalis bulla (Mammalia, Multituberculata) and its implications to mammalian evolution. Contr. Geol. Univ. Wyo. Spec. Paper 4: 1–104.Google Scholar
  51. Muller, M. and Verhagen, J. H. G. (1988). A new quantitative model of total endolymph flow in the system of semicircular ducts. J. Theor. Biol. 134: 473–501.Google Scholar
  52. Nomina Anatomica Veterinaria (1973). International Commission on Veterinary Anatomical Nomenclature, Adolf Holzhausen's Successors, Vienna.Google Scholar
  53. Olson, E. C. (1944). Origin of mammals based upon cranial morphology of the therapsid suborders. Geol. Soc. Am. Spec. Paper 55. Google Scholar
  54. Pritchard, U. (1881). The cochlea of Ornithorhynchus platypus compared with that of ordinary mammals and of birds. Phil. Trans. R. Soc. Lond. 172: 267–282.Google Scholar
  55. Quiroga, J. C. (1979). The inner ear of two cynodonts (Reptilia—Therapsida) and some comments on the evolution of the inner ear from pelycosaurs to mammals. Gegenbaurs Morph. Jb. 125: 178–190.Google Scholar
  56. Ramprashad, F., Landolt, J. P., Money, K. E., and Laufer, J. (1984). Dimensional analysis and dynamic response characterization of mammalian peripheral vestibular structures. Am. J. Anat. 169: 295–313.Google Scholar
  57. Rosowski, J. J. (1992). Hearing in transitional mammals: Predictions from the middle-ear anatomy and hearing capabilities of extant mammals. In: The Evolutionary Biology of Hearing, D. B. Webster, R. R. Fay, and A. N. Popper, eds., pp. 615–631, Springer Verlag, New York.Google Scholar
  58. Rosowski, J. J., and Graybeal, A. (1991). What did Morganucodon hear? Zool. J. Linn. Soc. 101: 131–168.Google Scholar
  59. Rougier, G. W., Wible, J. R., and Hopson, J. A. (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: 188–216.Google Scholar
  60. Rouger, G. W., Wible, J. R., and Hopson, J. A. (1996a). 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
  61. Rougier, G. W., Wible, J. R., and Novacek, M. J. (1996b). Middle-ear ossicles of the multituberculate Kryptobaatar from the Mongolian Late Cretaceous: Implications for mammaliamorph relationships and the evolution of the auditory apparatus. Am. Mus. Novitates 3187: 1–43.Google Scholar
  62. Rowe, T., Carlson, W., and Bottorff, W. (1993). Thrinaxodon, Digital atlas of the skull, CD-ROM, University of Texas Press, Austin.Google Scholar
  63. Simpson, G. G. (1933). The ear region and the foramina of the cynodont skull. Am. J. Sci. 26: 285–294.Google Scholar
  64. Spoor, F., Wood, B., and Zonneveld, F. (1994). Implications of early hominoid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369: 645–648.Google Scholar
  65. Starck, D. (1979). Vergleichende Anatomie der Wirbeltiere auf avolutionsbiologischer Grundlage, Bd. 2,XII, Springer-Verlag, Berlin.Google Scholar
  66. Turkewitzs, B. G. (1934). Anatomie des Gehörorgans der Vögel (Canales semicirculares). Z. Anat. Entwickl. 103: 551–608.Google Scholar
  67. Wall, C. E., and Krause, D. W. (1992). A biomechanical analysis of the masticatory apparatus of Ptilodus (Multituberculata). J. Vertebr. Paleontol. 12: 172–187.Google Scholar
  68. Watson, D. M. S. (1913). Further notes on the skull, brain, and organs of special sense of Diademodon. Ann. Mag. Nat. Hist. 12: 217–228.Google Scholar
  69. Werner, C. F. (1960). Das Gehörorgan der Wirbelthiere und des Menschen, Fischer Verlag, Jena.Google Scholar
  70. West, C. D. (1985). The relationship of the spiral turns of the cochlea and the length of the basilar membrane to the range of audible frequencies in ground dwelling mammals. J. Acoust. Soc. Am. 77: 1091–1101.Google Scholar
  71. Wever, E. G. and Lawrence, M. (1954). Physiological Acoustics, Princeton University Press, Princeton, NJ.Google Scholar
  72. Wible, J. R. (1990). Petrosals of Late Cretaceous marsupials from North America, and a cladistic analysis of the petrosal in therian mammals. J. Vertebr. Paleontol. 10: 183–205.Google Scholar
  73. Wible, J. R., and Hopson, J. (1993). Basicranial evidence for early mammal phylogeny. In: Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 45–62, Springer-Verlag, New York.Google Scholar
  74. Wible, J. R., Rougier, G. W., McKenna, M. C., and Novacek, M. J. (1997). Earliest eutherian ear region: A petrosal of Prokennalestes from the Early Cretaceous of Khoobur, Mongolia. J. Vertebr. Paleontol. 17(Suppl): 84A.Google Scholar

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  • Jørn H. Hurum

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