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The Rotatory Mobility of the Fibula in Eutherian Mammals by C

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The Rotatory Mobility of the Fibula in Eutherian Mammals by C [ 11 ] THE ROTATORY MOBILITY OF THE FIBULA IN EUTHERIAN MAMMALS BY C. H. BARNETT AND J. R. NAPIER Department of Anatomy, St Thomas's Hospital Medical School It is generally recognized that the rotatory mobility of the fibula varies considerably throughout the eutherian mammals. Little functional significance has been assigned to this variation, however, apart from the observation of Carleton (1941) that immobility of the fibula is characteristic of jumping, burrowing and swimming mammals, while mobility is confined to certain members of the Carnivora and the Primates. Walmsley (1918) came to the conclusion that the proximal end of the fibula existed mainly as a muscular process, while the distal end was the significant portion which owed its existence in a mobile form to the movements of the foot. Owen's view (1866) was similar, though more specific, when he stated 'it is to this prehensile power [of the foot] that the modifications of the fibula chiefly relate'. The authors (1952) have shown that, in man, the mobility of the fibula, as judged by the criteria of the shape, inclination and size of the superior tibio-fibular joint, is related to movement at the ankle and hence to the form of the talus. The fibula is mobile in those individuals in whom the axis of rotation at the ankle joint is steeply inclined, but is relatively immobile if this axis is horizontal. This finding in man suggests a method of approach to the wider problem of the functional significance of fibular mobility in other mammals. In the present investi- gation an attempt has been made to link mobility of the mammalian fibula with movements at the ankle during locomotion. MATERIALS AND METHODS Ninety-four species, comprising representatives from all the known orders of eutherian mammals with the exception of the Cetacea, Sirenia and Dermoptera, and including most of the important families, were examined. The specimens were, for the most part, in the form of disarticulated limb bones, but at least one wet specimen from each of the more common orders and suborders was dissected; these amounted to twenty-four in all and are indicated in Tables 1-3. Where rotatory mobility was anticipated the bones were stripped of all their muscles, leaving a ligamentous preparation of the two limb bones with the attached foot. Metal indicator pins were driven into each long bone and the relative divergence of these two pointers during passive movement, indicating rotation of the fibula relative to the tibia, was photo- graphed and measured. This rotation is usually extremely small, and it may easily be missed unless such a procedure is adopted. Measurements of the tali were made in accordance with the method employed for the human talus. The axis of the ankle joint was ascertained by finding central points of the circles of which the curvatures of the medial and lateral profiles of the talus form a part. 12 C. H. Barnett and J. R. Napier OBSERVATIONS The majority of fibulae could be classified according to the characteristics of the superior and inferior tibio-fibular joints into three distinct groups: the immobile, the mobile and the intermediate. (1) The immobile fibula, partly or wholly fused to the tibia, is widely represented among the mammals, and examples were found in all the orders examined, although the tarsier, Tarsius spectrum, is unique among the Primates (Table 1). There are Table 1. The immobile fibula (Where wet specimens have been examined they are indicated by an asterisk.) Superior Inferior tibio-fibular tibio-fibular Animal Order joint joint *Erinaceus europaeus (hedgehog) Insectivora Fused Fused Gymnura gymnura (gymnura) Insectivora Fused Fused *Sorex araneus (common shrew) Insectivora Synovial Fused Desmana moschata (Russian desman) Insectivora Fused Fused Potamogale velox (otter shrew) Insectivora Synovial Fused Macroscelides probosctdeus (common Insectivora Synovial Fused elephant shrew) Petrodromus tetradactylus (four- Insectivora Fused Fused toed elephant shrew) Rhynchocyon cirnei (long-nosed Insectivora Fused Fused jumping shrew) Centetes ecaudatus (tenrec) Insectivora Synovial Fused *Chrysochloris asiatica (cape golden Insectivora Fused Fused mole) Halichoerus grypus (grey seal) Carnivora Fused Syndesmosis Otaria californiana (sea-lion) Carnivora Fused Syndesmosis Procavia capensis (Cape coney) Hyracoidea Fused Fused P. syriaca (Syrian coney) Hyracoidea Fused Fused P. abyssinica (Abyssinian coney) Hyracoidea Fused Fused Dendrohyax dorsalis (Gold Coast Hyracoidea Fused Syndesmosis tree-coney) *Rattus norvegicus (bwown rat) Rodentia Synovial Fused *Mus musculus (house mouse) Rodentia Synovial Fused Bathyergus maritimus (African Rodentia Fused Fused sand-mole) *Cavia cobaya (guinea-pig) Rodentia Synovial Fused Jaculus jaculus (African jerboa) Rodentia Synovial Fused *Oryitolagus cuniculus (rabbit) Lagomorpha Synovial Fused Lepus europaeus (hare) Lagomorpha Synovial Fused Priodontes gigas (giant armadillo) Edentata Fused Fused Orycteropus afer (aard-vark) Tubulidentata Fused Syndesmosis *Tarsius spectrum (tarsier) Primates Synovial Fused two main varieties within this group: first, those showing bony fusion of the tibia and fibula at the upper end associated with fusion or an extensive fibrous tissue union at the lower (Figs. 1 and 2); and, secondly, those showing fusion at the lower end with a synovial joint at the upper (Fig. 3). Both types are associated with a talus the appearance of which is generally rather square, there being no splaying of the medial and lateral sides (Fig. 4A). The two profiles of the trochlear surface of the bone often show symmetrical and equal curvatures, so that the axis of movement at the ankle tends to be parallel to the plane of the trochlear surface and a true ginglymoid move- ment results. It may be seen from Table 1 that within the same zoological order the tibio-fibular articulations may show quite different characteristics. For example, the fused upper The rotatory mobility of the fibula in eutherian mammals 13 and lower tibio-fibular joints in the African sand-mole, Bathyergus maritimus, appear to make this species unique in this respect in its own particular order. Among the Hyracoidea, a synostosis at the upper end and a syndesmosis at the lower are typical of tree-livingvarieties, while asynostosis at bothends isfoundamongthefossorial coneys. On the other hand, similar tibio-fibular articulations are found in members of quite different orders; for example, a synovial joint at the upper end of the fibula with a Fig.*l Fig. 2 Fig. 3 Fig. 1. Cape golden mole (Chrysochloris asiatica). x 5. Fig. 2. Grey seal (Halichoerus grypus). x i. Fig. 3. African jerboa (Jaculus jaculus). x Ii. A B Fig. 4. Diagrams illustrating the relation of the axis at the ankle joint to the lateral articular surface of the talus. A, tali found in association with the immobile fibula-the axis may or may not be parallel to the upper surface; B, talus usually found in association with the mobile fibula. synostosis at the lower is found among many Insectivora (e.g. the European mole, Talpa europaea), in most members of the Rodentia and Lagomorpha (e.g. the jerboa, Jaculus jaculus, and the common rabbit, Oryctolagus cuniculus), and within the Primates (the tarsier, Tarsius spectrum). These observations suggest that identical forms of tibio-fibular articulation in diverse mammalian types are the results of functional adaptations and are independent of taxonomic considerations (Fig. 11). (2) The mobile fibula, where both upper and lower tibio-fibular joints are synovial, is found in only two orders, the Carnivora and the Primates (Table 2). 14 C. H. Barnett and J. R. Napier Table 2. The mobile fibula (Both the superior and the inferior tibio-fibular joints are synovial in all the species listed in the table. Where wet specimens have been examined they are indicated by an asterisk.) Order: Primates Order: Carnivora *Lemur catta (ring-tailed lemur) *Felis domesticus (domestic cat) L. fulvus (brown lemur) Panthera leo (lion) L. variegatus (ruffed lemur) *P. tigris (tiger) *Perodicticus potto (common potto) P. pardus (leopard) Cebus capucinus (capuchin) Lynx lynx (lynx) Ateles frontatus (spider monkey) *Lutra lutra (otter) *Macaca mulatta (Rhesus monkey) *Ailuropoda melanoleuca (giant panda) M. speciosa (stump-tailed macaque) *Selenarctos tibetanus (Himalayan M. nemestrina (pig-tailed macaque) black bear) Papio hamadryas (sacred baboon) Ursus arctos (brown bear) *P. cynocephalus (yellow baboon) Thalarctos maritimus (polar bear) P. anubis (anubis baboon) P. porcarius (chacma baboon) Mandrillus sphinx (mandrill) Hylobates hoolock (gibbon, hoolock) H. lar (gibbon, lar) Simia satyrus (orang-utan) *Pan troglodytes (chimpanzee) Gorilla gorilla (gorilla) In the twenty-nine species examined the upper articulation consisted of a large synovial joint, the lower of a short syndesmosis and, in addition, a large semilunar facet on the tibia covered by articular cartilage and in continuity with the ankle joint (Figs. 5 and 6). Rotatory mobility of this type of fibula was demonstrated by means of metal in- dicator pins driven into the shafts of the leg bones 1,, / in six wet specimens (chimpanzee, baboon, lemur, bear, tiger and cat) stripped of their muscles with their ligaments left intact. In chimpanzee, lemur and bear, the mobile phase of fibular movement occurs as the foot is passively dorsi-flexed from the neutral position. Complete separation of the bones is prevented by the tension in the posterior talo-fibular and transverse tibio- fibular ligaments, while the anterior talo-fibular and tibio-fibular ligaments are relaxed, allowing the fibula to hinge posteriorly. The movement of lateral / rotation can be demonstrated after all the ligaments have been divided provided the fibula is held in Fig. 5 Fig. 6 contact with the side of the talus-thus indicating Fig. 5. Orang-utan, Simia satyrus. that the main factor in producing the movements is x 1. the conformation of the lateral side of the talus. Fig. 6. Himalayan bear, Selen- aretos tibetanus. x -. In the cats and the baboon, on the other hand, fibular rotation is limited to the plantar-flexion phase, the bone undergoing a medial rotation as the foot is plantar-flexed from the neutral position.
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