• DGF OnLine Series

Jørn H. Hurum, Paleontologisk Museum, Sarsgt. 1, N-0562 Oslo, Norway

Introduction

Multituberculates, the rodents of the Mesozoic, thrived as the most successful group of mammals in the shadow of the dinosaurs. The small beasts have been found in deposits ranging from the late Triassic, early Jurassic or even late Jurassic, depending on the idea of what multituberculates are (see Kielan-Jaworowska in press for a review), to the late Eocene (Swisher & Prothero 1990). The earliest skull material is from the late Jurassic of Portugal (Hahn 1969) and is assigned to the suborder Paulchoffatoidea. Complete cranial remains of the suborder Taeniolabidoidea from the late Cretaceous of the Gobi Desert have been described in several papers (see Kielan-Jaworowska et al. 1986; Hurum 1994; Gambaryan & Kielan-Jaworowska 1995; Hurum et al. 1995 and references therein) and are the best known of the Mesozoic multituberculates. Several isolated petrosals and partial cranial remains are known from the Cretaceous, Paleocene and Eocene of North America of the suborders Ptiolodontoidea and Taenioloabidoidea, and of the suborder Taenioloabidoidea from Asia (see e.g. Wible & Hopson 1995 for further references). The inner ear of Mesozoic mammals has been described in a few papers, Morganucodon by Graybeal et al. (1989),Sinoconodon by Luo et al. (1995) and for multituberculates by Miao (1988), Luo & Ketten (1991) and Meng & Fox (1995).

The petrosal (os petrosum, periotic) represents an area of great interest in mammalian evolution. The cochlea, vestibule and semicircular canals, are bony cavities inside the petrosal containing the duct of cochlea, utricle and saccule, and semicircular ducts respectively. These are commonly known as the inner ear. The organs are for hearing, balance and orientation in space. In reptiles, birds and mammals, the cochlear duct, an elongated endolymphatic chamber, is in contact with the saccule. On the outer surface, the petrosal provides attachment areas for the muscles and ligaments of the ear ossicles. Several important cranial nerves pass through various openings in and around the petrosal. Nearby the internal carotid artery (to the brain) enters the skull and the internal jugular vein leaves it. The entire bone is formed as an endochondral ossification of the otic capsule. The petrosal is homologous with the reptilian prootic and opisthotic combined, and is fused in adult mammals. In extant eutherian mammals the petrosal is usually obscured by the tympanic bulla and situated behind and medial to the glenoid fossa. In multituberculates the petrosal bone forms a large part of the basicranium in ventral view. In lateral view the bone has an anterior lamina contributing to the lateral side of the cavum epiptericum and braincase. A large anterior lamina is shared with several other Mesozoic mammals (Sinoconodon, morganucodontids, triconodontids and Vincelestes, see Wible 1990).
Material and methods
The data for this work were obtained by study of serial sections from the skulls of two late Cretaceous multituberculates from the Gobi Desert,Chulsanbaatar vulgaris (ZPAL MgM-1/84) from the Red Beds of Khermeen Tsav and Nemegtbaatar gobiensis (ZPAL MgM-1/76) from the Barun Goyot formation. Both specimens were collected by the Polish-Mongolian Palaeontological Expeditions (1963-1971) and are deposited in the Institute of Paleobiology, Polish Academy of Science, Warsaw (abbreviatiated ZPAL). As both Nemegtbaatar gobiensis and Chulsanbaatar vulgaris are monotypic genera, I will use only the generic names Nemegtbaatar and Chulsanbaatar for brevity. The sections were made by Prof. Zofia Kielan-Jaworowska during her stay in the Institute de Paléontologie, Muséum National d’Historie Naturelle, Paris and the Department of Comparative Anatomy, University of Paris VII between 1982-1984. A Jung microtome was used. The wax model of the inner ear was also made during her stay. From the Chulsanbaatar skull, 885 sections 20 Tm thick were obtained, while from the Nemegtbaatar skull 1370 sections 25 Tm thick were obtained. Both sectioned skulls were given three reference marks through all sections (Kielan-Jaworowska et al. 1984; Kielan-Jaworowska et al. 1986, Hurum 1994). Photographs of every fifth section, taken in ultraviolet light, were enlarged 20 times. Models of the petrosal bone of both specimens were made using both photographs and sections. The sections were drawn on plastic plates and cut by a heating wire. The plastic used was Kappaplan 2 mm white plates. The cut pieces were glued to transparent film containing three reference marks. Sections were then glued together and the surrounding transparent film cut away. The models were then photographed, and the photographs over traced using a permanent ink marker, before bleaching to provide outlines.

The adult skull of Nemegtbaatar is estimated to be 40-45 mm long (Kielan-Jaworowska et al. 1986). In the sectioned skull the anterior part of the snout is missing and the length of the skull was 36 mm.

Chulsanbaatar is one of the smallest multituberculates with an adult length of the skull between 17-24 mm. The sectioned skull measured 17,7 mm and an adult skull is estimated at 21 mm (Kielan-Jaworowska et al. 1986).

Observations
One of the peculiar features of sectioned multituberculates is the thick bony medial wall of the cavum epiptericum, the taenia clino-orbitalis (ossified pila antotica). The cavum epiptericum is a large primitively extracranial space situated lateral to the sidewall of the orbitotemporal region of the skull. The space containins the post-trigeminal ganglion, primary head vein and several nerves (ophthalmic, oculomotor, trochlear, maxillary, mandibular and abducent, see Kielan-Jaworowska et al. 1986). In multituberculates it is separated medially from the cranial cavity by the taenia clino-orbitalis, bordered laterally by a small alisphenoid and the large anterior lamina, and floored by the petrosal (Kielan-Jaworowska et al. 1986; Hahn 1988; Miao 1988). The taenia clino-orbitalis was described as present as a reduced process inMorganucodon and Trioracodon (Hopson 1964), but new studies have rejected this (Wible & Hopson 1993). Absence of taenia clino-orbitalis (and pila antotica) is shared by triconodontids, Morganucodon, marsupials and eutherians (Wible 1990, Wible & Hopson 1993), where the boundary between the cavum epiptericum and the cranial cavity is indicated only in soft tissue by the dura mater (de Beer 1937). In Monotremes the cavum epiptericum is well defined, bordered medially in Tachyglossus by a bony taenia clino-orbitalis and laterally by the anterior prosess of the petrosal (Kielan-Jaworowska et al. 1986).

In the sectioned skulls, the cavity of the cochlear canal is well preserved and measurements of cochlear length have been made from the models and sections. The length of the cochlear canal in Nemegtbaatar is approximately 3,0 mm (Table 1) and for Chulsanbaatar 1,6 mm. The canal is straight and directed anteromedially as in most Mesozoic mammals (e. g. other multituberculates, Sinoconodon, triconodontids andMorganucodon), while in more derived Mesozoic mammals, like Vincelestes the cochlea curves to 270 (Rougier et al. 1992). The cochlear duct extends anteromedially and curves ventrally in monotremes (Ornithorhynchus 270 and Tachyglossus 180 ; Kermack et al. 1981, but see Meng & Fox 1995), and spirals into loops in extant therians. The ratios of cochlear canal length to skull length (cochlea/skull x 100%) are 6,7% and 7,6% for Nemegtbaatar and Chulsanbaatar respectively. Compared to other Mesozoic mammals (Luo et al. 1995), this is larger thanSinoconodon (2,7%) and Morganucodon (5,7-6,3%), smaller than Haldanodon (8,8%) and Catopsalis (8,1%); and Meniscoessus (7,3%) plots between the two.

The organ of equilibrium, the semicircular canals, exhibits few evolutionary changes through time (Lewis et al. 1985). From the model of the semicircular canals in Nemegtbaatar, the anterior canal is the largest and the lateral canal is somewhat larger than the posterior canal (Table 1). In Chulsanbaatar the semicircular canals are difficult to reconstruct because of distortion and poor preservation. In mammals generally, the anterior canal tends to be the largest of the semicircular canals and the lateral canal develops later than the anterior and posterior (Werner 1960). Curthoys et al. (1977) stated that only higher mammals have a fully developed lateral canal comparable in size to the others, but observations from the present work shows that multituberculates also had fully developed semicircular canal system.

Table 1. Measurements made from wax models and photographed sections of the inner ear of Nemegtbaatar gobiensis. Measurements were made on both sides and the mean values are shown. ASC – Anterior semicircular canal, LSC – Lateral semicircular canal, PSC – Posterior semicircular canal.

Conclusions
In the petrosal region, Rougier et al. (1992), distinguished mammals from non-mammalian cynodonts by the presence of a prootic canal with a tympanic aperture lateral to the secondary facial foramen in the roof of the lateral trough. The prootic canal is reduced or lost in marsupials and placentals where the postglenoid foramen takes over its function. Luo et al. (1995) added two apomorphies in the petrosal bone, an elongated cochlear canal and a petrosal promontorium. The prootic canal, the elongated cochlea and a petrosal promontorium are all present in multituberculates. The long cochlear canal and well developed semicircular canals observed in the sectioned skulls of Nemegtbaatar andChulsanbaatar, suggests close affinity of multituberculates to other mammals, and the thick ossified pila antotica suggests affinity to monotremes.
References

Curthoys, I. S., Blanks, R. H. I. & Markham, C. H. 1977: Semicircular canal radii of curvature (R) in cat, Guinea pig and man. Journal of Morphology 151, 1-16.
de Beer, G. 1937: The development of the vertebrate skull. Oxford University Press. 552 pp.
Gambaryan, P. P. & Kielan-Jaworowska, Z. 1995: Masticatory musculature of Asian taeniolabidoid multituberculate mammals. Acta Palaeontologica Polonica 40, 45-108.
Graybeal, A., Rosowski, J. J., Ketten, D. R. & Crompton, A. W. 1989: Inner-ear structure in Morganucodon, an early Jurassic mammal.Zoological Journal of the Linnean Society 96, 107-117.
Hahn, G. 1969. Beiträge zur Fauna der Grube Guimarota Nr 3, die Multituberculata. Palaeontographica, A 133, 1-100.
Hahn, G. 1988: Die Ohr-Region der Paulchoffatiidae (Multituberculata, Ober-Jura). Palaeovertebrata 18, 155-185.
Hopson, J. A. 1964: The braincase of the advanced mammal-like reptile Bienotherium. Postilla 87, 1-30.
Hurum, J. H. 1994: The snout and orbit of Mongolian multituberculates studied by serial sections. Acta Paleontologica Polonica 39,
Hurum, J. H., Presley, R. & Kielan-Jaworowska, Z., 1995: Multituberculate ear ossicles. In: A. Sun & Y. Wang (eds) Sixth Symposium on Mesozoic Terrestrial Ecosystems and Biota, Short Papers, 243-246.
Kermack, K. A., Mussett, F. & Rigney, H. W. 1981: The skull of Morganucodon. Zoological Journal of the Linnean Society 71(1), 1-158.
Kielan-Jaworowska, Z. (in press). Characters of multituberculates neglected in phylogenetic analyses of early mammals. Lethaia.
Kielan-Jaworowska, Z., Poplin, C., Presley, R. & de Riqlès, A. 1984: Preliminary data on multituberculate cranial anatomy studied by serial sections. In: W. -E. Reif & F. Westphal (eds) Third Symposium on Mesozoic Terrestrial Ecosystems, 123-128. Attempto Verlag, Tübingen.
Kielan-Jaworowska, Z., Presley, R. & Poplin, C. 1986: The cranial vascular system in taeniolabidoid multituberculate mammals. Philosophical Transactions of the Royal Society of London B 313, 525–602.
Lewis, R. E., Leverenz, E. L. & Bialek, W. S. 1985: The vertebrate inner ear. CRC Press Inc, Florida. 248 pp.
Luo, Z. & Ketten, D. R. 1991: CT scanning and computerized reconstructions of the inner ear of multituberculate mammals. Journal of Vertebrate Paleontology11(2), 220-228.
Luo, Z., Crompton, A. W. & Lucas, S. G. 1995: Evolutionary origins of the mammalian promontorium and cochlea. Journal of Vertebrate Paleontology 15 (1), 113-121.
Meng, J. & Fox, R. C.1995: Evolution of the inner ear from non-therians during the Mesozoic: Implications for mammalian phylogeny and hearing. In: A. Sun & Y. Wang (eds) Sixth Symposium on Mesozoic Terrestrial Ecosystems and Biota, Short Papers, 235-242
Miao, D. 1988: Skull morphology of Lambdopsalisbulla (Mammalia, Multituberculata) and its implications to mammalian evolution.Contributions to Geology, University of Wyoming, Special Paper 4, I-VIII + 1-104.
Rougier, G. W., Wible, J. R. & Hopson, J. A. 1992: Reconstruction of the cranial vessels in the early Cretaceous mammal Vincelestes neuquenianus: implications for the evolution of mammalian cranial system. Journal of Vertebrate Paleontology 12, 188-216.
Swisher, C. C. III & Prothero, D. R. 1990: Single–Crystal 40Ar/39Ar dating of the Eocene–Oligocene transition in North America. Science 249, 760-762.
Werner , C. F. 1960: Das Gehörorgan der Wirbelthiere und des Menschen. Fischer Verlag, Jena. 309 pp.
Wible, J. R. 1990: Petrosals of late Cretaceous marsupials from North America, and a cladistic analysis of the petrosal in therian mammals.Journal of Vertebrate Paleontology 1(2), 183-205.
Wible, J. R. & Hopson, J. A. 1995: Homologies of the prootic canal in mammals and non-mammalian cynodonts. Journal of Vertebrate Paleontology 15(2), 331-356.
Wible, J. R. & Hopson, J. 1993: Basicranial evidence for early mammal phylogeny. In: F. S. Szalay, M. J. Novacek & M. C. McKenna (eds):Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, 45-62. Springer Verlag, New York.