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The Auditory Apparatus of the Heteromyidae (Rodentia, Sciuromorpha) by ADE PYE Institute of Laryngology and Otology, London

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The Auditory Apparatus of the Heteromyidae (Rodentia, Sciuromorpha) by ADE PYE Institute of Laryngology and Otology, London J. Anat., Lond. (1965), 99, 1, pp. 161-174 161 With 3 plates and 7 text-figures Printed in Great Britain The auditory apparatus of the Heteromyidae (Rodentia, Sciuromorpha) BY ADE PYE Institute of Laryngology and Otology, London INTRODUCTION The family Heteromyidae possess many exceptional and interesting features for adaptation to life in the deserts. There are five living genera: Heteromys, Liomys and Perognathus, collectively known as the spiny pocket mice and rats, Dipodomys, the kangaroo rat, and Microdipodops, the kangaroo mouse. Despite their popular names these animals have no close affinity to the murid rats and mice; their closest relatives are the Geomyidae, the pocket gophers. All except Heteromys inhabit arid or semi-arid areas of North and Central America, while Heteromys is found further south and lives in rather swampy regions. Specializations in this family include bipedal locomotion, modified excretory system for conservation of body water, ability to withstand fluctuations between extremes of temperature and a greatly enlarged middle ear cavity. There are, however, at least four other families of small mammals whose members may inhabit deserts and have there developed similar characteristics. Three of these families belong to Rodentia: Muridae (e.g. Notomys- the Australian Jerboa rat), Dipodidae (e.g. Dipus the Jerboa of Asia and Africa) and Cricetidae (e.g. Gerbillus and Meriones, the Gerbils of Asia, North Africa and Eastern Europe). The fourth family, Dasyuridae, contains Antechinoinys, the marsupial 'Jerboa mouse' of Australia. Very little is known at present about the auditory problems facing these desert inhabitants. It is curious that this parallel evolution has occurred so many times in different families and in such widely separate geographical locations. Phylogeny of the Ileieromnyidae Webster (1960-61) discovered that the cochlea of Dipodoinys spectabilis and D. inerriamni has an unusual structure. The present author has continued and extended this study to cover all the five genera of Heteromyidae, concentrating mainly on the structure of the cochlea. These results may best be considered in relation to the phylogeny of the group. The evolutionary origin and later classification of the present-day rodents has given rise to a great deal of controversy and the Heteromyidae provide no exception. The early classifications were inadequate in many respects and Wood (1931) re- organized Heteromyidae, including both fossil and present-day representatives, mainly on the basis of the structure of their teeth. The living genera were thus divided into three main groups: 1. Ileteronmys and Liomys 2. Perognathus 3. Microdipodops and Dipodoinys 162 ADE PYE However, after the discovery of more fossil forms, Wood (1935) concluded that Microdipodops showed more affinities to Perognathus, especially in the foot struc- ture, than to Dipodornys. The following subfamilies were then founded: 1. Heteromyinac Heteromys and Liomys 2. Perognathinae Perognathus and Microdipodops 3. Dipodomyinae Dipodomys Xohen placing Microdipodops into the Perognathinae Wood stated that the animal has probably been a distinct phylogenetic line for a considerable time. Later Ellerman (1940-41) agreed with the above affinities, but reorganized the animals into only two subfamilies, putting Perognathus and Microdipodops into Dipodo- myinae. Simpson (1945), however, sided with Wood and their classification is used here. The evolutionary pattern is thus suggested to be: Dipodomys Microdipodops _1___<Perognathus Liomys Heteromys General account of ear structure The general structure of the human auditory apparatus has been excellently described by Shambaugh (1932). Accounts of the structure of the ears in rodents are given by Wassif (1948), Fernandez (1952) and many general histology books. Keen & Grobbelaar (1941) in a comparative survey of the mammalian tympanic bulla re- marked on its large size in the gerbil Desmodillus. Later, Meriones crassus was studied by Wisner et al. (1954), Legouix etal. (1955). Howell (1932) conductedastudy on the general gross anatomy of the Heteromyidae, including the ears. Webster (1960 a, b, 1961) followed this with an intensive account of the whole ear structure in two species of Dipodotnys. Pye (1964) has continued with a survey of the auditory apparatus in the whole family, of which this paper forms the first published account. MATE tItALS The species examined are as follows: Heteromys aorlnalus three specimens, Liornys pictus three specimens, Perogilathus californicus two specimens, Microdipodops pallidus two specimens, Dipodomys a itra- toides two specimens, Dipodomys agilis two specimens. HISTOLOGICAL TECHNIQUE Live specimens of all genera except Heterornys were sent to London from Cali- fornia by Dr Eisenberg of Berkeley University. Heterornys was obtained from the Regional Virus Laboratory, Port of Spain, during a visit to Trinidad. It was found by experience that the histological preparation of the ear, especially of the cochlea, required careful processing and the following method was found to be most suitable Auditory apparatus of Heteromyidae 163 (Pye, 1964). All the animals were treated alike. General anaesthesia was induced by an intraperitoneal injection of Nembutal (45 mg./kg.), so that the thorax could be opened. A cannula was introduced through an incision in the wall of the left ventricle and was tied into the dorsal aorta. The right auricle was punctured and the animal was perfused with Ringer or saline solution at body temperature. When all the blood had been washed out, Wittmaack's solution (formaldehyde, potassium dichromate, glacial acetic acid and distilled water) was forced through for immediate fixation of the tissues, which then turned a yellow colour. This intra-vitam fixation method was found to be the only way to obtain standard results of the internal ear and is similar to the technique used by Wisner et al. (1954). The head was then removed, skinned, trimmed down and placed in a fresh supply of the fixative, followed by Orth's solution, each for 1 day. Further fixation and leaching of the dichromate was achieved in frequent changes of formol calcium. Decalcification occurred in a 1 % solution of hydrochloric acid; the time taken for this to be com- pleted varied between 3 and 5 weeks, depending on the size of the head. After wash- ing in running and distilled water, dehydration through the alcohols was followed by the double embedding method of Peterfi (Carleton & Leach, 1947). First embedding occurred in three changes of 1 % celloidin methyl benzoate, clearing in benzene and second embedding in three changes of wax. Vacuum embedding was considered to be essential for the dispersion of gas bubbles, especially from the middle and inner ear cavities. The sections were cut in a horizontal plane at 7-8,a thickness and the primary stains used were haematoxylin and eosin in conjunction with periodic- acid-Schiff or Van Gieson's (Carleton (1943), Claydon (1955), Lulling (1957) and Steedman (1960)). Observations of the slides, measuring and photography were accomplished under a Zeiss Ultraphot photographic microscope. RESULTS The external ear. The external ear in all the Heteromyidae is simple in structure and small to medium in size. It appears to be largest in Heteromys. The middle ear. As the middle ear has been extensively studied by Howell (1932) and Webster (1960 a, b, 1961), this account will be kept to a minimum. The abnormal Multiple connective - tissue sheaths Stapes footplate Inner 9 Outer connective connective tissue sheath C tissue sheath Text-fig. 1. The footplate of the stapes in the oval window. Left: the inner and outer connective tissue sheaths in Heteromys. Right: the multiple connective tissue sheaths present in Dipodomys and Microdipodops. 11 Anat 99 164 ADE PYE inflation of the bulla is especially marked in Dipodomys, and Ellerman (1940-41) states that in Microdipodops this development is carried further than in any other rodent he examined (P1. 1, fig. 1). The auditory ossicles are small, as are the intra-aural muscles associated with them. The oval window opens into the scala vestibuli much higher up the cochlear spiral than inl other mammals (PI. 1, fig. 2). Another noticeable feature is that, in the more primitive members of this family, the stapes is secured in the oval window by only two sheaths of connective tissue, one internal and one external. In Dipodomnys and Microdip)odop0s these connexions are multiple (Text-fig. 1). Tlext-fig. 2. A schlematic drawing of the cochlea wh1ichl defines the measurements made and referred to in the text. B.Ml.W., basilar mlembrane width; B..lIT., basilar membrane thickness; (X.(:., the cells of Claudius: ARE, the hetwiht of the spiral ligament; CD, the width of the spiral ligament. Thle innere ear. After a lprelimlinary survey of the cochleae it has been discovered that some features change considerably in structure along the cochlear spiral and especially inlterspecifically. These features have been selected for measuring and will be discussed in turn (Text-fig". 2). They are: (I) The greatest height of the cochlea. ('2) The number of half-turnls present in the cochlea. (3) Radial measurements from the centre of the spiral ganglion to the outside of each turnl. (4) Central mleasulremnelts from the centre of the spiral ganglion to the inner rod of Corti. (5) The wsidlth of the basilar membrane from the lip of the spiral ligament to the inner rod of C8orti. (6) The greatest thickness of the basilar mlembrane. Auditory apparatus of Heteromyidae 165 (7) The greatest height of the spiral ligament. (8) The greatest width of the spiral ligament. All the graphs show the mean values for the number of cochleae examined, usually from four to six. It is realized, of course, that a larger number of animals would have been desirable. General form of the cochlea In all the Heteromyidae the general form of the cochlea is a truncated cone, except that the cochlea appears to have opened out markedly at the very base. The number of half-turns seen in horizontal section varies between seven and eight (PI.
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