LIBRARY OF THE UNIVERSITY OF ILLINOIS AT URBANA-CHAMPAIGN 590.5 FI V.5I cop. 3 SURVEY JkJk FIELDIANA • ZOOLOGY Published by FIELD MUSEUM OF NATURAL HISTORY Volume 51 February 20, 1970 No*4*— /(• Morphological Parallelisms of the Bulla and Auditory Ossicles in Some Insectivores and Marsupials Walter Segall Research Associate, Vertebrate Anatomy ABSTRACT Insectivores and marsupials show similar phylogenetic stages of morphological differentiation of the tympanic, entotympanic, and the malleus, which range from generalized (Solenodon-Didclpkis) to the highly specialized (Tupaia-Dromiciops) . In the insectivores the tympanic process of the basisphenoid takes the place of the tympanic process of the alisphenoid of the marsupials. The presence of an ento- tympanic suggests specialization in both orders. The malleus of marsupials and insectivores undergoes greater morphological changes than the incus. The ossicu- lar functional axis meets the horizontal in a large angle in the generalized taxa and shows a smaller angle and even a negative one in Dromiciops and the burrowing insectivores. Apparently, the malleus turned first, as was also shown for mar- supials (Segall, 1969b), other morphological changes followed later. This mor- phological sequence is probably caused by mechanical influences. In insectivores the stapes is characteristically and consistently specialized, unlike the two other ossicles, which show far greater differences. The marsupials show a greater range in the shape of the stapes, especially of the plate. Even if the stapes is not preserved, as is usually true in fossil specimens, the fenestra ovalis gives an accurate outline of the shape of the stapes plate and of its position. The shape of the latter or the fenestra ovalis in marsupials varies from practically round to oval in the more generalized and elliptical in the specialized taxa. In the insec- tivores generalized and specialized genera alike have stapes with elliptical plates. In the fossorial genera of both orders tympanic, malleus, incus, and the articu- lation between the latter two are markedly affected. However, the stapes retains the ordinal characteristics. The stapes of the insectivores has well-curved crura. In most genera the sta- pedial artery fills only a part of the intracrural space, which speaks for the inde- pendence of the two. Thus, it can be assumed that the function of the stapes is the most influential factor for determining its shape. The round outline of the stapes plate Cor fenestra ovalis) is considered the primitive condition, the elliptical the specialized one. Library of Congress Catalog Card Number: 77-115191 .......... KATURH HISTORY SURVEY No .1086 169 (^ MAR 12 1970 LIBRARY 170 /-TYM PANIC Fig. 22. Didelphis albiventris. Lateral view of right middle ear. and their close mechanical relationship. The changes in the tym- panic are probably primary due to its greater exposure to outside mechanical forces; those of the malleus secondary (Segall, 1969 b). A similar situation prevails in the insectivores. The malleus has a generalized form in the majority of the genera. The articulation is saddle-shaped, except in the Talpidae, Scalopinae, and Chrysochlori- dae, where it is much flatter. The neck of the malleus is long and shows a sharp bend in the generalized forms. In the more specialized Erinaceidae, the bend is reduced to a slight curve. The Talpidae have a nearly straight neck and in the Tupaiidae, the neck is practically missing. The lamina is large, thin, and quadrangular in the generalized genera. In the Talpinae it is much smaller, triangular, and laterally convex. In Condylura the lamina is somewhat rectangular, different from that in Talpa. The malleus of Tupaia has a very small lamina only. The reduction in the size of the lamina is approximately par- alleled by the reduction in length of the neck. The apophysis orbicularis is well developed in the generalized forms; becomes sessile, then indistinct in the more specialized genera; and finally disappears altogether. This can be well observed in the SEGALL: THE BULLA AND AUDITORY OSSICLES 199 INCUS Short Crus I Long Crus i \ ' CHORDA\ I FORTZATZ\.^" I MALLEUS I I I I Head I Capitular Crest I Anterior Process I MALLEUS / Neck' / / Short / Process/ Manubriunri Anterior Crus of Tympanic ^-' 3 mm Fig. 23, Dromiciops australis. Lateral view of right middle ear. Erinaceidae, where Hylomis and Echinosorex, which represent the more generahzed genera, have a well-developed apophysis orbicularis while the more specialized Erinaceus and Hemiechinus have only an indication of it. There is none in the Talpidae. The disappearance of the apophysis orbicularis goes parallel with the straightening of the neck. A similar condition of the lamina and apophysis orbicularis can be seen in the marsupials (Segall, 1969b). The angle between the neck and manubrium is antero-ventrally and slightly medially directed in some families. In Erinaceus and Hemiechinus the angle is open antero-ventrally and veiy much me- dially. In Tupaia the membrana tympani with the manubrium stands in a nearly vertical plane and the head of the malleus is severely bent medially against the latter. The mallei in both orders with very generalized auditory regions, as in Solenodon (fig. 4) and in Didelphis (fig. 22), are very sim- 200 FIELDIANA: ZOOLOGY, VOLUME 51 ilar to each other. The same appHes to genera with very specialized auditory regions like those in Tupaia (fig. 21) and Dromiciops (fig. 23.) Incus The incus shows, in general, few morphological differences in the various families. The posterior crus is short in the generalized taxa and its posterior end rests in most genera in the epitympanic recess; only in the most specialized ones does it reach into a fossa incudis in the posterior wall of the cavum tympani. The modification of the incus in the fossorial genera is striking. This can be seen in the in- sec tivores (Talpa, fig. 18 and Chrysochloris, fig. 10b) as well as in marsupials (Notoryctes, figs. 3, 3A). The position of the short crus is a determining factor in the direc- tion of the ossicular functional axis (see Methods and Material) . The angle between the ossicular functional axis and the horizontal plane tends to be greater in the generalized forms. Viewed from the right side, the axis turns with increased specialization counterclockwise and the angle with the horizontal plane becomes successively smaller and even negative (fig. 24). A similar turning of the ossicular func- tional axis can be observed in the marsupials (Segall, 1969 b). At a certain stage of rotation of the ossicular functional axis a change in the morphology of the malleus takes place. This is pre- sumably a phyletic response to changing mechanical requirements. In Hylomys, where the angle of the axis with the horizontal is already reduced to about 27°, the malleus has still preserved its generalized form. In Erinaceus and Hemiechimis, however, wheve the angle is reduced to about 20°, the malleus shows morphological changes. These changes become marked when the angle comes close to the zero point, as in Talpa. This is especially true in Tupaia in which the differentiation of the malleus is similar to that of the primates. A similar condition occurs in Dromiciops among the marsupials (Segall, 1969 a). The similarity among fossorial genera applies to the external ap- pearance of the auditory region and to the articulation between malleus and incus. Both characters are presumably- correlated by a modified function in subterranean environment. Stapes The insectivore stapes does not change to any extent with pro- gressive specialization of the auditory region, in contrast to malleus and incus. Even in the highly specialized Talpinae and still more in ...1 '^^ 0RY20RICTCS <•* », "^^< 'V ^N-*^ ^%, ^», ^ 4 0°'X HORIZONTAL ago-^^ POTOMOQALE ECHINOSOREX V ECHINOPS -^ SliTlrEi^ TENREC SOLENODON CLEPHANTULUS CR1NACCU3 HEMIECKINUS UROPSILUS TALPA CONDVLURA SCAPANUS EUROSCAPTOn Fig. 24. The angle of the ossicular functional axis with the horizontal plane in insectivores. 201 202 FIELDIANA: ZOOLOGY, VOLUME 51 Fig. 25. Tachyglossa aculcata. Ventral view of periotic. the Chrysochloridae, where the malleus and the incus have a unique morphology, the stapes does not differ from that of other insectivores. The near constancy of the stapes ratio of the plate (or the fenestra ovalis) is of taxonomic interest, especially in fossils. Furthermore, the position of the plate or the fenestra ovalis, with regard to the horizontal plane is of comparative anatomical interest in closely related forms. Both the position and the shape of the sta- pedial plate can contribute to the identification of fossils. For ex- ample, the foramen ovale of the fossil erinaceoid genus Ictops (fig. 14) has a stapedial ratio and position identical to those of Erinaceus (fig. 26). A primitive form of mammalian stapes is found in the mono- tremes. This type of stapes has a columella without opening (sta- pedial foramen) and a circular plate (stapes ratio 1.0, fig. 25). The marsupials, in which some genera approach the monotremes in this respect while others are much advanced, have stapedial plates with ratios ranging from 1.1 to 2.1. With progressive specialization of the auditory region the stapes ratio increases in marsupials (fig. 26). SEGALL: THE BULLA AND AUDITORY OSSICLES 208 TUPAIA I 8CALOPUS D SOLENOOON ORYZORICTES NESOPMONTES. ERINACEUS. ICTOPS TENREC, ELEPHANTULUS. SOREX HYLOMIS DROMICIOPS, MACROPUS PETAURUS 1.7 1.6 TACHVGLOSSUS D PMALANGER, D VOMBATUS. AEPYPRYMNUS I I CALUROMYS, OENOROLAGUS. PHILANDER - II NOTORYCTES. PERAMELES. MARMOSA I I ECMYMIPERA, METACHIRUS. OIOELPHI8 - ' □ i.a ANTECHINUS. SMINTMOP8I8 I I DASYURU8 • Fig. 26. The stapedial ratio: a, in monotremes (below); b, in marsupials (right side); c, in insectivores (left side). At the same time, the space between the crura (absent in the columella-like stapes) enlarges only slightly in the marsupials, while the stapes plate may expand considerably. The stapedial foramen in marsupials, if present at all, is always small and never reaches the size commonly observed in insectivores. 204 FIELDIANA: ZOOLOGY, VOLUME 51 In Notoryctes the malleus and incus have a morphology that is quite different from that of any other marsupial (fig. 3). The stapes, however, retains its marsupial character. It has a flat columella with a shallow groove at the base, but no canal. Specialization of malleus and incus, but not of the stapes, may be related to the fossorial habit of Notoryctes. The same two elements are modified in fossorial in- sestivores (Talpinae and Chrysochloridae), while the stapes retains its typical insectivore character. The morphology of the stapedial plate changes first, that of the crura afterward. It is presumably the function that determines the configuration of the plate. The presence, absence, or degree of de- velopment of the stapedial artery is not directly correlated with the size of the opening between the crura and it only occasionally fills it completely. The round shape of the plate and fenestra ovalis is a primitive mammalian character; the elliptical shape, a specialized one. The pi'esent study has shown that the stapes is characteristic in each of the two orders of mammals considered. In the marsupials there is a progressive specialization of the stapes from a columella- like form with a round plate to a stapes with a small opening between the crura and an elliptical plate, while in the insectivores it is invari- ably stirrup-shaped, irrespective of the general level of specialization of the genus. In contrast, the ectotympanic, malleus, and incus in both orders show similar, parallel, progressive morphological changes with overall increase of specialization of the genera. In both orders, furthermore, fossorial genera show marked devia- tions from the typical condition of malleus and incus, but not of the stapes. It was suggested that these profound changes are related to the fossorial habits. ACKNOWLEDGEMENTS I am grateful to Dr. S. Anderson for the loan of a Notoryctes typhlops skull and Dr. R. H. Tedford for five Nesophontes skulls and for reviewing this paper. Field Museum placed the entire mammal collection at my dis- posal. I am especially indebted to Dr. William Turnbull, Dr. R. Zangerl, and Dr. K. Liem for their generous help. In addition, I would like to thank Mr. W. Boyer and Mr. S. Grove for the illustra- tions and Mr. H. Holden for his gi'eat effort with the photographic work. I also thank Miss J. L. Williams for typing the manuscript. SEGALL: THE BULLA AND AUDITORY OSSICLES 206 REFERENCES DORAN, A. H. G. 1877. Morphology of the mammalian ossicula auditus. Trans. Linn. See. Lon- don, 1, pp. 371-497. Kampen, p. N. van 1905. Tympanalgegend des Saugetierschadels. Morph. Jahrb., 34, pp. 321-722. Segall, W. 1969a. The middle ear region of Dromiciops. Acta anat. 73, no. 4, pp. 481- 501. 1969 b. The auditory ossicles (malleus, incus) and their relationship to the tympanic in marsupials. Acta anat. 73, no. 2, pp. 176-191. Simpson, G. G. 1945. The principles of classification and a classification of mammals. Bull. Amer. Mus. Nat. Hist., 85, 350 pp. Weber, M. 1928. Die Saugetiere. Gustav Fischer, Jena. <;