1 [ 225 ] SOME FACTORS INFLUENCING ANGULATION OF THE NECK OF THE MAMMALIAN TALUS BY C. H. BARNETT Department of Anatomy, St Thomas's Hospital Medical School INTRODUCTION The degree of angulation of the talar neck varies greatly from one mammalian species to another, and it would be expected that this diversity has either a functional or a taxonomic significance. From his exhaustive study of the mammalian talus, Volkov (1904) concluded that the angle of the neck has a 'quite exceptional importance' in assessing the functions of the foot, while Duckworth (1904) has stated that 'this character distinguishes the Hominidae clearly from the Simiidae...'. In an attempt to determine the reason for this structural variation, a number of tali have been examined, particular attention being paid to the different factors that could have influenced the angle of the neck during the course of evolution. MATERIAL AND METHODS Ninety-eight adult mammalian limbs have been studied, including twenty-five wet specimens. In addition, thirty-five human feet have been examined from twenty cadavers and fifteen post-mortem subjects. The angle of the neck of the talus is commonly determined by laying the disarticulated bone upon a horizontal plane and measuring the angle between the long axis of the neck and that of the trochlear surface, as seen from above. Although this is a convenient method (Inkster, 1927), it has two serious defects. In many animals the trochlear margins are not straight and the neck is short with irregularly shaped sides. Consistent figures are then very difficult to obtain. An even more serious source of error, as Appleton (1913) emphasized, is that the orientation of the talus in the living foot is seldom identical with that of the excised bone placed on a horizontal surface. Since the neck is usually inclined downward as well as medially, slight changes in the orientation of the bone may cause apparent alterations in the talar angle. For this reason, measurements of the angle have been recorded mainly in wet specimens or in dried osteoligamentous preparations of the whole foot. A large talar angle could be produced either by medial deviation of the neck within the foot or by obliquity of the trochlear margins. The latter might be caused by obliquity of the trochlear margins only, the upper surface of the talus forming part of a screw (Fig. 1), or alternatively by deviation of the whole trochlear surface, with a consequent obliquity of the axis of rotation at the ankle joint. These three theoretical possibilities are shown in Fig. 2. To assess which of these factors was responsible for a large angle of the neck in any specimen, the long axis of the foot was first determined by joining the middle of the forefoot-or, in pentadactyl limbs, the middle digit-to the mid-point of the heel.
2 226 (7. H. Barnett Fig. 1. Left foot of wallaby. The trochlea is part of a right-handed screw set transversely in the foot. A BC Fig. 2. Three factors affecting the angle of the talar neck: A: medial deviation of the neck relative to the long axis of the foot; B: obliquity of the trochlear margins relative to the long axis of the foot; C: deviation of the trochlear surface, and the axis of rotation at the ankle joint, relative to the long axis of the foot.
3 Factors influencing angulation of neck of mammalian talus 227 The direction of the long axis of the talar neck, the plane of the trochlear margins and the position of the axis of rotation at the ankle joint were then determined relative to the long axis of the foot. The ankle joint axis was deduced from the contours of the medial and lateral profiles of the talus as previously described (Barnett & Napier, 1952, 1953). So far as possible all the tarsal joints were maintained in the neutral position during the measurements. OBSERVATIONS AND DISCUSSION The simplest type of talus is one in which the long axis of the neck and both trochlear margins are parallel to the long axis of the foot, which is itself at right angles to the axis of rotation at the ankle joint. This type, with no angulation of the neck, is found characteristically in species with a long narrow foot adapted for a cursorial type of gait, such as the rabbit (Oryctolagus cuniculus), rabbit bandicoot (Thalacomys lagotis), tiger-cat (Dasyurus maculatus), Tasmanian devil (Sarcophilus harrisi) and many of the cursorial artiodactyla. Table 1 indicates the relative importance of the three factors-medial deviation of the neck, obliquity of the trochlear margins, and deviation of the whole trochlea with a corresponding obliquity of the axis of rotation at the ankle joint-in forty species with a large talar angle. Medial deviation of the neck This is an important factor in increasing the talar angle in two types of animals. Firstly, it occurs in those in which the force transmitted down the leg is deviated within the foot towards its medial side, as in arboreal forms with a prehensile hallux. Secondly, it is present in animals with a wide foot in which the head of the talus lies to the medial side of the calcaneum, a relationship of the two proximal tarsal bones which is commonly found in animals with a burrowing habit or a plantigrade gait (Table 1). Obliquity of the trochlear margins In those species in which the trochlear surface forms part of a screw, there may be considerable lateral movement of the talus upon the tibia during flexion and extension at the ankle joint, especially if the obliquity of the trochlear margins and the total range of ankle movement are both large. It can be shown by a modification of Manter's method (1941) that in the horse, for example, the talus moves bodily about 4 mm. in a lateral direction as it passes from full dorsiflexion to full plantarflexion. A screw type of articulation is very stable, being especially well suited to resist antero-posterior strains. While some of the animals with this type of talus are heavy, active creatures with elongated limbs, capable of jumping, they do not all possess ankle joints that palpably require especial protection against such strains. Moreover, the actual pitch of the screw varies greatly even in those creatures that conform to this pattern; consequently the angle of the neck may differ in related species (e.g. lion, tiger) due solely to differences in the pitch of the screw of which the trochlea is part.
4 228 C. H. Barnett Table 1. The factors responsible for a large talar angle in forty species No. of Total Medial Obliquity of Deviation specimens Type of angle of deviation trochlear of ankle Species examined specimen talar neck of neck margins axis Castor fiber (beaver) 2 O.L Centetes ecaudatus (tenrec) 2 O.L Tarsius spectrum (tarsier) 3 W Chiromys madagascariensis (aye-aye) 1 O.L Hapale jacchus (marmoset) 2 WV Mandrillus sphinx (mandrill) 3 B Procavia capensis (Cape coney) 3 WV Mustela erminea (stoat) 1 W Panthera leo (lion) 3 B Tapirus indicus (tapir) 2 B Equus caballus (horse) 3 B Pedetes cafer (jumping hare) 1 O.L Macropus rufogriseus (wallaby) 2 WV Dendrolagus matschei (tree-kangaroo) 1 IV Potorous tridactylus (rat kangaroo) 1 W Dendrohyrax dorsalis (tree-coney) 3 O.L Hydrochoerus hydrochoeris (capybara) 2 B Hystrix cristata (porcupine) 3 W Chrysochloris asiatica (golden mole) 2 WV Erinaceus europaeus (hedgehog) 3 W Bathyergus maritimus (sand-mole) 2 O.L Canis familiaris (dog) 5 W Ailuropoda melanoleuca (giant panda) 2 B Meles meles (badger) 2 NV Priodontes gigas (giant armadillo) 2 B Ateles frontatus (spider monkey) 2 W Cercocebus collars (mangabey) 1 WV Mystax ursulus (tamarin) 1 O.L Macaca mulatta (rhesus monkey) 4 XV Hylobates hoolock (gibbon) 2 O.L Papio papio (guinea baboon) 3 W Simia satyrus (orang utan) 3 B Gorilla gorilla (gorilla) 3 B Homo sapiens (man) 35 W Tamandua tetradactyla (lesser ant-eater) 2 O.L Panthera tigris (tiger) 3 B Myrmecophaga jubata (giant ant-eater) 2 B Felis domestic (cat) 4 IV Myocaster coypus (coypu) 2 O.L Orycteropus afer (aardvark) 2 W O.L.: osteoligamentous preparations studied; W.: at least 1 wet specimen studied also; B.: only dried bones seen. In the first fifteen species listed, only one factor is responsible for the large talar angle; in the remainder at least two factors play a part. Deviation of the ankle axis In most species the axis of rotation at the ankle joint is transverse, i.e., at right angles to the long axis of the foot. In certain arboreal forms the ankle axis is oblique, usually lying approximately parallel to the line joining the heads of the lateral four metatarsal bones. In man also, it has been shown by modifications of Manter's method (Manter, 1941; Barnett, 1953; Hicks, 1953) that the ankle axis is not usually at right angles to the long axis of the foot as is often stated (e.g., Elftman & Manter, 1935; Wood Jones, 1949), but is directed backwards and laterally, so that a line at right angles to it makes an angle of 5 to 10 degrees with the long axis of the foot. This lateral deviation of the trochlea in man is partly masked by a medially directed obliquity of the trochlear margins relative to the ankle axis (Table 1). Thus the
5 Factors influencing angulation of neck of nammnlian talus 229 human left talus may be regarded as part of a left-handed screw the long axis of which points backwards and laterally* (Fig. 3). The obliquity of the human ankle axis is in large measure the cause of the supination of the foot that accompanies plantarflexion; this rotational movement is only slightly reduced in patients whose subtalar and midtarsal joints have been arthrodesed. Some fossorial animals exhibit a similar deviation of the ankle axis from the transverse position, leading to marked supination-or, in certain instances, pronation-of the foot during plantarflexion. This rotational movement is probably of value in burrowing. Fig. 3. Left foot (human). The trochlea is part of a left-handed screw set obliquely in the foot (compare Fig. 1). CONCLUSIONS Since several distinct factors have influenced the angle of the talar neck during the course of evolution, the magnitude of the angle in any species is in itself useless as a guide to function unless the relative importance of these factors has been analysed. A very small talar angle is typical of cursorial forms. Medial deviation of the neck within the foot is found in species with a wide foot, for example, those with a plantigrade gait or a fossorial habit, and in arboreal species in which the body weight is deviated within the foot towards the medial side. A talus in which the trochlear margins are obliquely set within the foot is seen characteristically but not exclusively in heavy animals capable of jumping. A foot in which the whole trochlea, and thus the axis of rotation at the ankle joint, is deviated with respect to the long axis of the foot is found in some arboreal primates, and also in man and certain fossorial species. As the extensive studies of Matthew (1937) make clear, the tarsal bones are not uncommonly preserved intact in fossil form, and it may be that a reassessment of fossil tali along the lines suggested would throw some light on the habits of extinct fauna. * The analogy is admittedly imperfect: the axis of rotation at the human ankle is not, in fact, stationary. 15 Anat. 89
6 230 C. H. Barnett SUMMARY 1. Ninety-eight mammalian tali, representing forty-eight species, have been examined with respect to the degree of angulation of the neck. 2. Estimates of the talar angle may be misleading, not only because of fallacies and difficulties in the technique commonly adopted for its measurement, but because three distinct factors may be responsible for a large angle. 3. In forty species with a large talar angle, the relative importance of these factors is listed, and the functional significance of each of the three is discussed. I am indebted to Prof. D. V. Davies, the late Prof. F. Wood Jones, Dr F. C. Fraser and Miss J. E. King for helpful advice and for the provision of material. REFERENCES APPLETON, A. B. (1913). Note on a variable feature of the astragalus. J. Anat., Lond., 47, BARNETT, C. H. (1953). Further observations upon the axis of rotation at the human ankle joint. Proc. Anat. Soc. G.B.I., in J. Anat., Lond., 87, 449. BARNETT, C. H. & NAPIER, J. R. (1952). The axis of rotation at the ankle joint. J. Anat., Lond., 86, 1-9. BARNETT, C. H. & NAPIER, J. R. (1953). The rotatory mobility of the fibula in eutherian mammals. J. Anat., Lond., 87, DUCKWORTH, W. L. H. (1904). Morphology and Anthropology. Cambridge University Press. ELFrMAN, H. & MANTER, J. (1935). The evolution of the human foot, with special reference to the joints. J. Anat., Lond., 70, Hicus, J. H. (1953). The mechanics of the foot: I. The joints. J. Anat., Lond., 87, INKSTER, R. G. (1927). The form of the talus. Thesis. Edinburgh University. JONES, F. WOOD (1949). Structure and Function as seen in the Foot, 2nd ed. London: BailliLere, Tindall and Cox. MANTER, J. T. (1941). Movements of the subtalar and transverse tarsal joints. Anat. Rec. 80, MATTHEW, W. D. (1937). Paleocene faunas of the San Juan Basin, New Mexico. Trans. Amer. phil. Soc., N.S., 30. VOLKOV, T. (1904). Variations squelettiques du pied chez les primates et dans les races humaines. Bull. Soc. Anthrop. Paris, Ser. 5, 4,