the description of mammals–2 limbs and locomotion of terrestial mammals

Mammal Review Volume 3 Number 4 December 1973

The description of mammals-2 Limbs and locomotion of terrestial mammals J. CLEVEDON BROWN Department of Applied Biology, University of Cambridge

D. W. YALDEN Department of Zoology, University of Manchester

CONTENTS Introduction General descriptive terminology The characteristics of the mammalian limb Adaptive radiation .

General adaptations Stance

External charadters of ihe limb' Digits Claws, nails and hooves : Vibrissae and glands. Foot pads and dermatoglyphics

Foot pads and the definition of stance . Osteological identifications . Gaits . Discussion . References .

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. 108 . 110 . 111 . 112

. 113 . i i 5

. 117 . 119 . 121

. 122 . 124 . 125 . 126 . 128 . 132

ABSTRACT Four separate categories of description relating to limbs and locomotion are recognized. Gross variation in limb structure characterizes descriptions at the ordinal level. Detailed morphology of the external features, and of limb bones, extends diagnosis to the familial and generic levels. The gaits of mammals describe locomotory behaviour.

In all of these categories, definitions tend to be imprecise and the terminology to be mis- applied. This descriptive terminology is critically reviewed in the light of advancing research and a synthetic framework for ordering future studies is proposed.

INTRODUCTION This series of articles on the description of mammals is concerned with characters and terms used in the taxonomic classification, and subsequent identification, of mammals. It is actually a concern with descriptive nomenclature in a broader sense, since many of the terms have applications beyond those of characterizing and diagnosing specimens. Many of the characters, and the terms used to describe them, are poorly defined or imperfectly understood. One aim of these articles is to collate and define this terminology.

Many of the characters used must originally have been chosen, and subsequently become established in validity and usefulness, in an empirical manner. A knowledge of their biological significances is essential if the characters are to be used with real confidence. A second aim, therefore, is to examine these characters in the light of advancing research and, at the same time, to indicate fields in which new studies are needed.

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108 J. Clevedon Brown and D. W. Yalden

Mammalian classification has been described as a matter of teeth and feet. While this is an over-simplification it is true that dental characters, together with those of the skull, and characters of the feet and limbs are those most frequently employed. There are several reasons for this. Compared with other vertebrate groups, mammals generally conform very closely to a common pattern of skeletal structure. Dental morphology, as an adaptation to differing feeding regimes, shows considerable variation and is of fundamental importance in mammalian taxonomy. A degree of variation is also shown by mammalian limbs as a response to various locomotory adaptations. While this variation is less apparent than in the teeth, it is sufficiently marked to provide a basis for distinguishing some taxa at the ordinal and, in some cases, generic levels. Fossil mammals, with rare exceptions, are only represented by hard parts. Teeth are particularly valuable in this respect because of their resistance to decay and because of their variability. Foot bones and the articular ends of limb bones often preserve well and also provide valuable diagnostic features. For extant, living, mammals there are many other organs, including soft parts, which would be of equal value for diagnostic purposes but, in general, the emphasis in taxonomic practice has remained on dental and limb characters. This, perhaps, is as much due to the ‘skins and skulls’ tradition of museum collections as to maintaining a study approach suitable for both fossil and living material. Skins and skulls preserve a wealth of conventional taxonomic features, can be stored dry, and take up a minimum of valuable museum storage space. Characters of the feet rather than of the whole limb are, of course, of greater importance when working from museum skins.

Limb characters are clearly of importance in mammalian systematics, second only to dental characters. In terms of museum taxonomy per se, they are perhaps, a rather poor second but the importance of limbs is considerably enhanced when field descriptions and identifications are taken into account. Limb function, that is, locomotion, is perhaps the most obvious aspect of behaviour and, in field studies, particular patterns and tricks of locomotion provide essential diagnostic characters.

In fact, one can recognize four separate categories, and levels, of descriptive analysis relating to limbs. At the grossest level of analysis, mammalian limb structure and function is characterized by contrast with other vertebrates and the broad variations on this characteristic form provide features typifying taxa at, generally, the ordinal and family level. An important corollary of these features is the description of the way in which these varieties of limb structure support the animal. These provide the terms of stance which are often loosely and inaccurately applied. The next two categories of description involve detailed morphology of the limb. In one category are studies of the external characters of the feet of mammals which have a considerable importance in taxonomic studies, at least for some orders. The other category concerns skeletal characters, particularly of the carpal and tarsal bones and of the articular ends of the long bones, which, as already indicated, are of great value in the identification of mammalian remains in palaeontological and archaeological contexts. Features used in these two categories often relate to generic, sometimes even to specific, identification. The fourth category of analysis is that describing locomotory behaviour-the gaits of mammals.

These four categories of description are really quite disparate and have been developed largely in isolation one from another. They are not mutually exclusive but at their current level of development are hardly complementary. In our discussion we attempt to put them into perspective within an overall synthesis of researches on mammalian limbs and locomotion. It is not our aim to present an exhaustive review of the very extensive work within this field but rather to look for a unifying concept which might provide pointers for redirecting research. Particularly we have in mind the commoner, less specialized, species of mammals in which differences of anatomy and physiology are not obvious while, nevertheless, there are very evident differences of locomotory behaviour.

GENERAL DESCRIPTIVE TERMINOLOGY Description of mammalian limbs is bedevilled by the use of loosely defined terms, and, indeed,

Limbs and locomotion of terrestrial mammals 109

(tlOltj3dNI=) tlOltl31SOd

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by their misuse. A further complication is introduced by the fact that many comparative anatomists began their training with human anatomy. Compared with other mammals, Homo has many peculiarities and the established medical terminology is not always applicable to quadrupedal mammals. We have illustrated some of the less ambiguous terms in Fig. 1. Particular care is needed when describing the feet. The human hand is normally described in supination, so that its palm is anterior; in a rat the palmar surface would be ventral, and, in a horse, posterior. The alternative term flexor for the hand is accurately descriptive, but, in the foot, the flexor muscles (those on the flexor or plantar surface) actually cause extension of the joints! These difficulties become more acute when one attempts to compare some animal of bizarre anatomy and limb orientation (e.g. a mole or a bat) with more normal forms. It is not possible to lay down any ‘correct’ or ‘best’ terminology for such cases. The only safe rule is to redefine the terms for each instance. This applies equally to the terms used for movements at a joint. The terms flexion, extension, and hyper-extension are clear enough, but abduction and adduction (towards or away from the body) can be used ambiguously. In human anatomy, abduction of the hand would be a deviation to the ulnar side of the arm, whereas in most mammals it would mean radial deviation.

THE CHARACTERISTICS OF THE MAMMALIAN LIMB One of the distinguishing characteristics of mammals, with a few exceptions, is the manner in which the body is supported by the limbs. Amphibians and reptiles have a sprawling gait. The limbs are held more or less at right angles to the longitudinal axis of the body, strongly flexed at the elbow and knee joints which point upwards and outwards, and hardly lifting the belly from the ground. At rest, there is a tendency for the body to settle on the ground. Mammals, by contrast, have their limbs so disposed that the feet are placed immediately beneath the body and this is usually lifted well clear of the ground, even at rest (Fig. 2). Evolving from the reptilian condition, the mammalian limbs have been brought much closer in beneath the body so that the elbow joint points backwards and the knee joint forwards. In the forelimb this condition is achieved by a progressive torsion of the limb which is evident in the skeleton. Rotation of the hindlimb is achieved principally by changes in the anatomy of the hip joint. In the, basically quadrupedal, mammals both pairs of limbs have been realigned. Many groups of Ruling reptiles, including the birds, also evolved a hindlimb in which the knee faced forwards, but this was often associated with a bipedal locomotion.

The evolution of the characteristic mammalian limb posture is also closely related to changes in the limb girdles and, of great significance, changes in the vertebral column. Lateral sinuosity of the backbone is a major component in the locomotion of lower vertebrates and is seen, in exaggerated form, in the limbless eels and snakes. In mammals a new role has been evolved for the backbone. Lateral sinuosity is reduced and the vertebrae and trunk musculature form, instead, a relatively rigid compression member, generally bowed upwards, and in which movement is most marked in the dorso-ventral plane (Gregory, 1937) (Fig. 2). This dorso-ventral flexion is the prime locomotory movement in Cetacea (Slijper, 1961), but ‘inchworm’ flexing of the backbone also plays a very important part in, for example, the galloping of the cheetah, Acinonyx (Hildebrand, 1959).

With the reptilian form of limb, three methods of propulsion are possible. Axial rotation of the femur and humerus will, if the lower limb is held at right angles, drive the animal forwards. Amongst mammals, this action appears to be used by the monotremes (Howell, 1937; Jenkins, 1970, 1971) and may account for their retention of a sprawled limb disposition amongst their many reptilian features. The forelimb in moles also uses this action (Reed, 1951 ; Yalden, 1966) but in this case it is probably a secondary adaptation to the burrowing habit.

Retraction of the humerus and femur will also propel the body forwards, as will extension of the knee and ankle joints once the limb is retracted. These two actions are most efficiently

Limbs and locomotion of terrestrial mammals 11 I

Fig. 2.

combined in a more vertical limb pose and are the forms of propulsion used by the majority of terrestrial mammals. The characteristics of the mammalian limb are commonly summarized in terms of vertical limbs, that is, straight props underpinning the body, and moving in a parasagittal plane, i.e. fore and aft, like pendulums. This is, as Jenkins (1971) has observed, an over-generalization even for the extreme forms of mammal (those best adapted for fast movement) on which it is based. All mammals show a degree of flexion at the limb joints which is extremely variable, greater or lesser, depending on the mammal in question. The degree to which the limbs are disposed in relation to the longitudinal axis of the body is also variable and there is always a tendency to lateral excursion in movement, that is, they swing outwards past one another as Gregory (1912) pointed out long ago (see also, Yalden, 1971). There are real differences between reptilian and mammalian limbs but the mammalian limb cannot be characterized in a summary of a few words; the matter is too complex. As compared with the primitive reptilian condition, there is a tendency in mammals for the limbs to be brought into a position closer to the side of the body, for the feet to be planted close under the body, and for the limbs to move much more in a parasagittal, fore and aft, plane.

ADAPTIVE RADIATION The earliest known mammals, from the Mesozoic, were of small size, similar to that of living shrews and the smaller rodents (Clemens, 1970). Comparative studies indicate that the ancestral mammals were of nocturnal habit. They can be imagined as small, active, animals

Diagrammatic representations of stance in (a) an amphibian, (b) a reptile, and (c) a mammal.


living among rocks and thick vegetation or wherever the cover afforded a measure of pro- tection; a regime typical of a majority of small extant mammals. Burrowing and arboreal habits must have been early developed and, indeed, there is evidence that the earliest mar- supials (Cretaceous) were arboreal (Haines, 1958). The close of the Mesozoic saw the dramatic decline of the Ruling reptiles and in the succeeding Cenozoic era the previously obscure mammals underwent a rapid and wide ranging radiation. The reasons for this reversal of fortunes are not clear (for recent discussions see Cox, 1967 and Robinson, 1971) but certainly new environments were open to exploitation during the Cenozoic-‘the age of mammals’- particularly the wide grass-covered plains of steppe and savannah type. The exploitation of this new habitat by mammals required many adaptations, one of which was the adaptation of the limbs for speedy locomotion; speed to catch potential prey or speed to avoid potential predators.

The precise nature of these adaptations depends on the mammal under consideration. Of the two methods of propulsion mentioned earlier (p. IIO), retraction of the limbs results in an action somewhat like the swinging of a pendulum and uses energy primarily in over- coming the inertia of the limb. At the end of each swing the limb must be stopped and accelerated in the opposite direction. This is what Gray (1944), in his now classical biomechanical analysis of limb function, described as the use of limbs as levers.

The form of propulsion in which the intrinsic joints of the limb are alternately flexed and extended (what Gray termed the use of the limbs as extensible struts) involves less expenditure of energy in swinging the legs but it results in a bouncy form of locomotion in which the whole mass of the body is raised and lowered so that energy is used in shifting the centre of gravity of the body as its mass is moved up and down.

Smith & Savage (1956) have pointed out that, for a large mammal, using energy in bouncing the centre of gravity about is an extravagant means of locomotion; swinging the legs back and forth is more economical since a large animal can take longer strides. Conversely, for a small mammal, raising and lowering the centre of gravity uses less energy than swinging the legs. These factors are important in interpreting limb shape and stance.

General adaptations The terms used to describe the general locomotor adaptations of mammals are not intended to be used as precise terms, but have a useful descriptive function. Although used loosely they do indicate general characteristics of major groups of mammals. The primitive small mammal of our previous discussion probably walked, rather than galloped or hopped, and, in a word, was ambulatory. Many insectivores and rodents could still be so described.

Adaptation to speedier locomotion, using the leg-swinging form of propulsion, leads to a cursorial (literally, ‘running’) mammal, exemplified by many of the extant Carnivora, the Artiodactyla and the Perissodactyla. Some basically cursorial mammals are so heavy that their limbs and locomotion are further modified for weight bearing; these are described as graviportuf (e.g. Proboscidea). The alternative method of moving faster, using the extension of the joints, leads to bipedal hopping or saltatorial forms. Mostly these are small mammals, such as kangaroo-rats (Dipodomys), jerboas (Dipodidae) and bush babies (Gulugo), but the kangaroos (Macropodidae), some of which are large, are also saltatorial.

Not all groups of mammals have adapted to faster locomotion. The Primates are primarily tree-living, arboreal, forms. Some arboreal mammals are little adapted, morphologically, for that mode of life (e.g. Tupaiidae), but others show marked adaptations for climbing and are described as scansorial (e.g. sloths, Bradypodidae). Yet other mammals are adapted for burrowing e.g. moles, Talpidae, and Golden moles, Chrysochloridae. Burrowing mammals are described as fossoriaf, although this term is often given an extended meaning to include mammals which simply live in holes. Aquatic mammals are adapted for swimming and are described as natatorial, while the Chiroptera are volant or flying mammals. The last term may also be used to include gliding forms.

Limbs and locomotion of terrestrial mammals 1 13

Stance Small mammals, and some larger ones which do not require high speed, appear flat-footed or plantigrade (Fig. 3) . Propulsion is, with some exceptions, of the flexion-extension type and at the beginning of a cycle of movement the hindfoot is flat on the ground with the intrinsic joints of the limb flexed. In this position the maximum effect of extending the ankle joint is given at the beginning of the stride (a cycle of movement). Obvious examples include the hares and rabbits (Leporidae) and various mice (e.g. Apodemus, Peromyscus). Use of the ankle joint in this way has been greatly developed and refined in the bipedal, saltatorial, mammals (Badoux, 1965; Hall-Craggs, 1965). All of these have plantigrade hind limbs but so do some larger, non-saltatorial, forms, such as bears (Ursidae) and men (Hominidae) which use the more economical limb swinging form of locomotion. Why these large, leg- swinging forms should be plantigrade is not clear; it may simply be due to the retention of the primitive stance amongst the mosaic of generalized and advanced characters to be found in varying degrees in all mammals, or it might be adaptive in, for example, providing greater stability. Certainly they are not adapted for speed.

Fig. 3. The three categories of stance: (a) plantigrade (bear); (b) digitigrade (dog); (c) unguligrade (pig). After Howell, 1944.

As just intimated, the leg-swinging form of locomotion is more generally associated with larger and faster cursorial mammals. Cursorial mammals achieve greater speed by increasing the effective length of their limbs and so increasing the length of their reach. Many mammals,


including the majority of the Carnivora and some Rodentia, have realized this by becoming digitigrade; they walk on their toes thus adding the length of the foot to the distal segment of the limb. Indeed, many plantigrade mammals (including man) rise on to their toes when running, becoming temporarily digitigrade.

In associating the evolution of digitigrady with the assumption of cursorial, limb swinging, types of locomotion, we find ourselves in disagreement with Gray (1944). He developed a geometrical argument for believing that the digitigrade limb relieved the tension in certain muscles. This argument overlooked the fact that the plantigrade limb is often designed to use just these tensions for a joint-extension type of limb action and that a digitigrade limb may also exploit these same tensions; it is an analysis which worked only for a static limb and not for one in propulsive use.

The terms plantigrade and digitigrade have been much misused. For instance, both bears (Ursidae) and baboons (Papio, Mandrillus) are described as plantigrade animals. In both cases this is true of their hindlimbs only; their forelimbs are clearly digitigrade. A similar mistake is often made with regard to animals with short feet. The badger (Mefes), for instance, has been described as plantigrade (Neal, 1948) when it is, in fact, digitigrade as a careful comparison of its footprints with those of undoubted digitigrade carnivores would show (Fig. 15). In part, these confusions arise because the terms plantigrade and digitigrade are names for broad categories, loosely defined in a subjective manner, rather than by objective

Fig. 4. Hindlimb skeletons of (a) a plantigrade, (b) a digitigrade, and (c) an unguligrade mammal to show the changes in proportions of limb segments with change of stance.


reference to precise characters. Precise definitions can be made in terms of the plantar pads and we propose these below (p. 124).

The effective length of the limb can be increased further by rising on to the tips of the toes and achieving the unguligrade condition of hooved mammals such as cattle (Bovidae) and horses (Equidae). I t is these mammals which most closely approach the concept of ‘vertical limbs with a parasagittal excursion’. The limb is lengthened, not only by standing on ‘tiptoe’, but also by lengthening the limb overall. This lengthening of unguligrade limbs is associated, in varying degrees, with changes in the proportions of the limb segments (Fig. 4). While the proximal segment (the humerus or femur) remains relatively unchanged in length, the other segments show a progressive increase in their lengths from proximal to distal; the weightbearing foot bones show the greatest relative elongation. The efficiency of the limb as a pendulum depends on two other factors besides increase in length. As many of its joints as possible must be moved in the same direction at the same time or, more simply, the limb is straightened as far as possible and swung in as near a parasagittal plane as possible. Also, reduction of the weight of the lower limb will help to reduce the energy needed to overcome the momentum of the limb when it is swung. Thus, unguligrade limbs show marked adaptations of bone and joint morphology which ensure movement in only the desired plane of excursion. The repertoire of intrinsic movements of the limb is thereby severely restricted and the muscles responsible for the unwanted movements can be lost. Muscle weight in the lower limb is still further reduced by operating the adapted, fixed-movement, joints largely by tendons while, in the upper limb, the muscles needed to swing the limb pendulum-fashion, are concentrated proximally, close to the limb girdle. An incidental consequence of tendons operating the joints is the development in many unguligrade mammals of passive stay mechanisms which enable them to stand for long periods with the expenditure of little or no energy (see, for instance, Hofmann, 1966). These mechanisms, coupled with these animals’ peculiar light-sleep characteristics (Ashby, 1972) have a high survival value in allowing the animals to rest without loss of awareness of the surroundings and ready for instant movement.

There are two major variants of the unguligrade limb which name and partly define two orders of mammals, the Artiodactyla and the Perissodactyla. In the Perissodactyla weight is distributed about the middle digit and the side toes are variably reduced. This is the mesaxonic condition, seen in extreme development in the horse, Equus, where only the middle toe remains (Figs. 5, 6). A similar condition was reached in the extinct liptotern, Thoarherium. In the paraxonic condition, characteristic of Artiodactyla, the axis of the foot passes between toes 3 and 4 and both of these remain functional. The first digit is usually lost but the remaining two digits (2 and 5) may vary from well developed (e.g. Hippopotamus) to completely lost (e.g. Girafa) (Figs. 7, 8 ) . Some mammals may have mesaxonic hind feet and paraxonic front feet (e.g. the capybara, Hydrochoerus) while at least one (Choeropus, the pig-footed bandicoot) has mesaxonic front feet and paraxonic hind feet (Fig. 9).

The primitive axis of the foot presumably passed through the middle digit as in the mesaxonic condition. The observed orfunctional axis often differs from this. If it is shifted to the outside of the foot, as it is, for instance, in the paraxonic condition, the autopod is described as ectaxonic ; a shift of axis medially is termed entaxonic.

Non-functional toes may be evident as vestiges, the splint bones of the skeleton and the dew claws of the whole animal (Figs. 6, 8).

The straightening of the foot in cursorial mammals does not minimize the importance of the ankle joint. This is automatically flexed as the foot meets the ground so as to cushion the impact of the foot fall. It is almost immediately re-extended so initiating another cycle of movement. The highly developed biomechanical adaptations achieving this rapid flexion- extension are graphically described by Hildebrand (1960).

EXTERNAL CHARACTERS OF THE LIMBS External characters of the limbs, particularly of the feet, have a considerable importance in


3 (a) (b)

Fig. 5. Examples of mesaxonic feet: (a) raccoon; (b) man; (c) tapir. After Grass6 (1967).

Fig. 6. The mesaxonic condition: stages in the evolution of the limb in the Equidae. After Grass6 (1967).


(b) (C) . . Fig. 7.

taxonomic studies especially for the Carnivora and the Primates. The emphasis on these two orders must be due, in large part, to the influence of Pocock whose extensive researches pioneered this field of study and whose particular interests were in these orders.

Digits Primitively, the mammalian foot has five digits, that is, it conforms to the basic tetrapod pentadactyl condition. For descriptive purposes these digits are numbered from 1 the inner- most, to 5 the outermost. The first digit is distinguished by special names, the pollex for the thumb and hallux, for the big toe. The names indicus, medius, annularis and minimus for the other fingers of the human hand are not used for other mammals. The first digit, primitively, has only two phalanges whereas each of the others has three. This pattern is variable and is expressed as a phalangeal formula; the basic one being 2-3-3-3-3. The first digit also tends to be somewhat offset from the others with a potential for independent mobility. This seems to be an ancestral character (Lewis, 1964).

In addition to the loss of digits, a notable tendency in unguligrade mammals, the relative lengths of the digits represented is variable. Generally, in the mesaxonic condition the third is the longest, the second and fourth are about equal, the fifth somewhat shorter than these, and the first the shortest. The human hand conforms to this pattern. These relative lengths of the digits can be expressed as a digital formula. For the human hand it would be 3>2 = 4> 5 > 1, where > means ‘longer than’ and = means ‘same length as’. Pocock often refers to mesaxonic feet as perissodactyl, irrespective of whether they be plantigrade, digitigrade or unguligrade. Similarly he uses artiodactyl to describe paraxonic feet in which 3 = 4. These adjectives may be logical but they can be a source of confusion to the uninitiated.

Examples of paraxonic feet: (a) thylacine; (b)-hyaena; (c) deer. After Grass6 (1967).

(a) (b) (c) (d) Fig. 8. Series of fore feet of artiodactyls showing reduction of lateral digits: (a) pig; (b)chevrotain;(c)deer;

(d) cow.

3

(C)

3

Fig. 9. Paraxonic and mesaxonic feet in the same animals. (a) paraxonichind foot (Choeropus); (b) paraxonic front foot (Hydrochoerus); (c) mesaxonic front foot (Choeropus); (d) mesaxonic hind foot (Hydro- choerud.


Claws, nails and hooves The tips of the digits in tetrapods are, characteristically, sheathed with claws. Nearly all mammals have retained claws or developed the peculiarly mammalian variants, nails or hooves. Claws must be considered the archetypal form on the basis of palaeontological studies (Romer, 1966) and from studies in comparative anatomy (Clark, 1936). Like hairs, claws are kera- tinized structures produced from specialized regions of the germinal (Malpighian) layer of the epidermis. Such a specialized region is termed a germinal matrix in both claw and hair growth. A typical claw partially encloses the end of a digit, closely covering its top and sides, sheathing the distal portion of the terminal phalanx which is itself clawlike in shape, and projecting in a curved and pointed shape beyond the tip of the digit. To the curved and sickle-like shape is owed the latinized term for a claw-falcula. Claws are compressed laterally so that there is a narrow groove in the undersurface. This groove is filled with a softer, less cornified, tissue variously referred to as the sole-plate, sole-pad or subunguis. This tissue forms a zone of transition from the hard nail-plate to the normal epidermis of the undersurface of the digit. This zone may also be referred to as the hyponychium. Dorsally the nail-plate passes back to the root where it merges insensibly with the triangular shaped area of the germinal matrix. The root is protected by a fold of the integument known as the eponychium and in some species the terminal phalanx also has developed a protective bony flange (Ewer, 1973). Clark (1936) showed that the keratin of a typical claw is in two layers. The thinner, superficial, layer has the keratin lamellae orientated horizontally and these originate in the proximal part of the germinal matrix. The thicker, deeper, layer has more vertically disposed lamellae which originate from a more distal part of the matrix (Fig. 10).

Fig. 10. The structure of the typical claw. After Clark (1936).

Nails are particularly distinctive of Primates and are essentially reduced claws, flattened and broadened to cover only the dorsal surface of the tip of the digit. They are practically flat in the longitudinal plane and only slightly convex transversely. A latin term which has been used for this structure is ungula (but see below) while tegula refers to the more longitudinally curved and laterally compressed nails of, e.g. Platyrrhina, which in appearance are intermediate between nails and claws. Some Primates, lemurs, Tarsius, Hapalidae, Callimico, have more obviously claw-like structures while at least one nonprimate, the marsupial Caenolestes, has nail-like structures. The real difference between nails and claws, according to Clark (1936) depends on histological structure. In nails only the thinner, superficial layer is present; the deeper layer and the distal part of the germinal matrix are lacking. The germinal matrix of a nail is, therefore, broad and rounded (cf. the lunula-white crescent-of the


human nail), while the terminal phalanx is blunt and the nail does not project significantly beyond the digital pad. In these terms the claw-like structures of some Primates are found to be closer to nails than to claws (Clark, 1936; Hill, 1955).

Nails are, in every sense, reduced claws and are much weaker since the grasping strength of claws depends mainly on the deeper keratinous layer. We do not know whether the nails of Caenolestes have been examined histologically.

Mammals with claws or nails are described as unguiculate, a term sometimes misused in anthropologically based primate studies. Unguligrade mammals protect the tips of the functional toes with hooves and are termed ungulate. The hoof is also a modified claw which is shortened and broadened to form an incomplete cylindrical sheath for the toe-tip (Fig. 1 I). The distal end of this rests on the ground and the subunguis forms a pad within its curve- the sole of the hoof. The term ungula has also been used for the hoof, particularly in veterinary studies. An alternative name for the nail in the same genre could be unguis plunus (Weber, 1927). The latin forms are to be found in the literature; the english terms are unambiguous and are to be preferred for current usage.

Fig. 11. Schematic representations of a nail (left), a claw (middle) and a hoof (right) in ventral view (above) and longitudinal section (below). n, nail plate; e, eponychium; su, subunguis; dp, digital pad. After Weber, 1927.

Unguligrade mammals are, almost by definition, ungulate but not all ungulate mammals are necessarily unguligrade. Since the hooved mammals have evolved from unguiculate ancestors, many extinct forms showed intermediate developments while, among the Artiodactyla, the Agriochoeridae redeveloped claws and the Chalicotheriidae had well-developed claws although in all other characters they were typical Perissodactyla. All extant Artiodactyla are ungulate;


the Camelidae alone are exceptional in being not strictly unguligrade. Among the extant Perissodactyla the Equidae show extreme unguligrade and ungulate adaptation. The tapirs and rhinoceroses are, however, much more generalized and rather intermediate in hoof development. This emphasizes a real dichotomy in the Perissodactyla as pointed out by Simpson (1945). Mammals of orders other than Artiodactyla and Perissodactyla may be ungulate, for instance, the capybara, Hydrochoerus, among the rodents, and a number of fossil mammals of several orders. Ungulata as a super-ordinal term is properly obsolete (Simpson, 1945) but used loosely ‘ungulates’ is a convenient collective noun for the extant Artiodactyla and Perissodactyla.

As far as we are aware, there has been no real study of the morphogenetic mechanisms involved in the production of claws, nails and hooves and this would seem to be field for new studies.

Vibrissae and glands Vibrissae, similar to those of the face, may occur on the limbs. Four groups have been named (Jones, 1923) (Fig. 12). On the forelimb vibrissae may be anconeal (near the elbow), medial antebrachial (on the forearm), or ulnar carpal (just above the wrist), and, on the hindlimb, calcaneal (on the inside of the ankle). These vibrissae do not seem to have been much reported since the early notice by Beddard (1902) who recorded the occurrence of carpal and tarsal tufts in species of a number of orders. Pocock frequently illustrates these distal groups but without accompanying textual comments. One assumes that their function is similar to that of the facial vibrissae (Brown, 1971) and could therefore be of some interest in ethological studies. Some of the vibrissal groups may, on the other hand, be associated with specialized skin glands.

Medial antebrachial

/ - Ulnar carpal - Fig. 12. Position and nomenclature of vibrissae of the fore limbs. After Jones, 1923.

122 J . Clevedon Brown and D. W. Yalden

The latter deserve separate discussion with the skin glands as a whole, since this is an important and expanding field of study. We may note in passing that skin glands, of varying degrees of specialization and in varying positions from the axilla to the plantar surfaces, are to be found in the limbs of numerous species of mammals. From the point of view of taxonomic studies the most important have probably been the metatarsal (ankle) glands of deer and the interdigital glandr between the hooves of many artiodactyl species (Pocock, 1910).

Foot pads and dermatoglyphics The plantar surfaces are friction surfaces and are cornified to varying degrees of thickness. Cornification is greatest where most pressure is borne and the dermis, also, is thickened at these points to form cushions of dense connective tissue which serve to buttress the deeper lying skeletal elements and protect them from dislocation (Fig. 13). The areas of thickening

Digital I Pad Interdigital

The cushioning of the toe joints by foot pads in an digitigrade mammal. pads

Fig. 13.

are generally discrete, since an overall thickening of the sole would restrict the capacity of the foot for intrinsic movements. They form the foot pads. On a basic, plantigrade, foot there are three sets of pads (Fig. 14). Near the tip of each digit there is an apical or digital pad; at the bases of the phalanges, between the digits and covering the phalangeo-metapodial joints, are interdigital pads; and more proximally, near the wrist (metacarpal pads) or ankle (metatarsal pads) are a pair of pads of which the medial (inner) is termed the thenar and the lateral the hypothenar. The interdigital pads are sometimes called the plantar pads (Pocock) but the latter term is more useful as a collective term for all the foot pads. These points take the weight when the foot is placed on the ground; as the foot is lifting, the weight is progressively concentrated on the forward pads so that the final thrust is given from the digital pads. This pattern of foot pads is readily modified in response to adaptive changes in the functioning of the foot and this variability makes the foot pad pattern an extremely valuable taxonomic character. It has been used, not only for distinguishing between closely related species, but also to assign newly discovered species to their correct family or superfamily.


Fig. 14. The descriptive terminology of the foot pads. After Jones, 1923.

The skin between the pads may be haired, or naked and glandular, to varying degrees. Overgrowth of the sole by hair can be a climatic adaptation, as, for instance, amongst the bears (Pocock, 1914). The Lagomorpha are curious in that the interdigital, metacarpal and metatarsal pads tend to be lost and to be replaced by thick mats of hair. The extreme condition is typical of all Leporidae and the growth of hair seems to vary very little between species irrespective of climatic zone. The Ochotonidae (pikas) appear to be more intermediate in this trend (Pocock, 1925). Pads tend to be lost in arboreal mammals; thus, in those Primates in which the feet have a grasping function the pads tend to be lost, the skin to be glandular and to be sculptured into characteristic patterns of ridges and papillae-dermatoglyphics-of which human fingerprints are a familiar example. Dermatoglyphics are discussed in the first of this series of papers (Brown, 1971).

Of Pocock’s long series of papers, those dealing with the external characters of the feet of Carnivora are excellently summarized by Ewer (1 973) who also gives a good summary of claw functions in Carnivora. Data on the external characters of the hands and feet of Primates are reviewed in detail by Hill (1954 et seq.). Studies of other groups are both incomplete and widely scattered in the literature.


FOOT PADS AND DEFINITIONS OF STANCE The terms of stance are easily understood in theory but are often difficult to apply in practice. There is always some element of doubt about the accuracy of detail in the reconstruction of articulated skeletons. Museum specimens, whether dry skins or wet preserves, suffer various distortions which may lead to wrong interpretations. However, manipulation of freshly dead material and careful observations of the live animal and of its tracks are ideals which cannot always be realized.

The foot pads quite sensitively record changes in foot function; the metatarsal pads of Carnivora, for instance, are reduced with only a partial development of the digitigrade stance. Foot pads would appear to provide a means of proposing precise and practical definitions of the terms of stance, viz.: Plantigrade-the weight is borne by the digital, interdigital, thenar and hypothenar pads; digit 1 is sometimes lacking, when interdigital pad 1 also disappears or fuses with 2; fusions of pads and occasional subdivision of pads may occur in response to particular weightbearing stresses. Digitigrade-the weight is borne on the digital and interdigital pads; the thenar and hypothenar pads are reduced or lost (Fig. 15).

DI

14

Fig. 15. Drawings of the left hind footprints of a plantigrade (Myocasfor) and three digitigrade mammals, showing the relationship between footprints and stance. The three digitigrade examples show progressive fusion of the interdigital pads.


Unguligrade-the weight is carried by the terminal phalanges by way of their claws, hooves, and/or digital pads. Some would restrict the term to those mammals walking on the claws or hooves only and use the term sub-unguligrade for those (e.g. Camelidae, Tapiridae, Rhinocerotidae) where digital pads are involved.

Caution is still required when working from dried skins; Pocock frequently published corrections of conclusions reached from imperfect dried skins when freshly dead material later came to hand.

OSTEOLOGICAL IDENTIFICATIONS There is an immense literature on the osteology of the mammals. From these detailed comparative studies are derived the generalizations on the evolution and radiation of the mammalian limb which have been mentioned earlier. The descriptive terminology for these studies is that of comparative and veterinary anatomy and derives, ultimately, from the terminology earlier established in human anatomy. Apart from a very few terms for common and obvious adaptations, such as cannon-bone for the fused metapodials 3 and 4 of Artiodactyla, there are no names which would not be familiar to a student of human anatomy. Yet obviously the mammalian limb skeleton shows very considerable variations and not the least from the human condition. Beyond this standard terminology, description is in terms of relative proportions, reductions and fusions, spatial relationships of limb bones and the relative development of articular and muscle attachment processes. Saunders & Manton (1 969) give a useful introduction to, and summary of, the major variations at the ordinal level. Flower’s (1870) classic is still a useful reference and the volumes edited by Grass6 (1955; 1967) collate a great deal of detailed information. Cornwall (1956), Reed (1963), and Ryder (1969) give useful introductions to the practice of osteological identification. At a more refined level of diagnosis, illustrations better express differences than do words; atlases (e.g. Hue, 1907; Schmid, 1972) are extremely useful up to a point. That point is normally identification at the generic level, especially when fragmentary palaeontological or archaeological material is under consideration. Beyond this level the only certain method of procedure is direct comparison with known museum specimens.

This approach is essentially typological; the most useful bones and fragments are those with complex articular surfaces which are searched for distinctive and diagnostic features. Boessneck’s (1969) discussion of the skeletal differences between sheep and goat is a good example of the degree of detailed study involved. This sort of analysis is particularly required in the contexts of Quaternary and archaeological studies where the interest lies in the total fauna or faunal assemblage, its relationship to contemporary man and/or its value for deducing information about the past environment. An important corollary is the attempt to use osteological characters as evidence for the domestication of animals by man. There has, in these studies, been a natural bias towards the ungulates, as being important food animals of man, and to the larger carnivores, as being predators of man and competitors for the same prey animals. At the same time, these are groups showing advanced locomotory adaptations which aid identification and, perhaps, their study has become self-propagating, Until recently, little attention has been paid, in the typological approach, to the possibility of individual variation, clinal variation, age variations, or sexual dimorphism, nor has much thought been given to the functional significance of the characters used so that their value as phylogenetic indicators must be uncertain.

Intraspecific variation has recently been taken more into account. KurtCn’s (1968) review of European Pleistocene mammals is an important source for references of advances in this field, Evaluations of variation in modern related species is increasingly included in studies of fossil primate material, as, for instance, Oxnard’s (1968a) study of the fragmentary scapula from Sterkfontein and the Olduvai clavicle (1968b). The same procedure has been followed with studies of prehistoric cattle remains (Hodgson, 1968; Higham & Message, 1969). Un- doubtedly, great advances in this field will result from the application of multivariate statistics,


since these can simultaneously allow for variation within and between samples. In this, primatologists are in the lead. As an example, various analyses of the shoulder region (Oxnard, 1969; Oxnard & Neely, 1969) could fruitfully be taken as a model by other comparative anatomists and Oxnard’s (1968~) exposition of a method of investigation, while explicitly for studies of primate evolution, deserves wider application. There is also a move towards far more critical analysis of mixed assemblages of bones in archaeological contexts (Payne, 1972).

As regards the functional significance of the morphological differences used at this level of identification there are very few studies and a great scope for further work. This is needed, not only to give validity to empirically determined diagnostic features, but also because the features probably represent real functional differences expressing the ecological separations which enable different species to fit into the ecosystem. Schaeffer (1947) made a start in new studies, with a functional analysis of the artiodactyl astragalus. More recently, several papers have been published on the functional morphology of the carpus in various mammalian groups (Lewis, 1965, 1972; Yalden, 1970, 1971, 1972). In primatological studies the application of multivariate statistical analysis by Ashton & Oxnard (1964) successfully indicated functional features of the scapula and, as already mentioned, this promises to be a valuable approach for future work.

The need for a new assessment of osteological identifications taking account of variation and functional adaptation, has been expressed in another quarter. Earlier ideas on how domestication might effect morphology (summarized by Zeuner, 1963) led to the establishment of osteological criteria for distinguishing between wild and domestic representatives of species, particularly in remains from early sites which might yield evidence for the origins of domestication. The whole concept of domestication has been discussed recently and, in particular, the validity of morphological criteria for recognizing domesticated animals has been critically assessed and brought into question (Bokonyi, 1969; Chaplin, 1969; Herre, 1969; Higgs & Jarman, 1972; Jarman & Wilkinson, 1972).

GAITS Despite the development of slow motion cinematography the description of mammalian gaits is still in its infancy. Classic terms, derived usually from equestrian practice, tend still to be used, often with little or no precision. A suitable introduction to such terms is provided by Muybridge (1899, reprinted 1957), while Howell (1944) adds more discussion. We include here only a brief outline of the topic to meet our terms of reference. The accompanying review by Dr Dagg summarizes the more recent literature on mammalian gaits.

Muybridge (1957) recognized eight basic mammalian gaits, viz. walk, amble, trot, rack, cunter, transverse gallop, rotary gallop and ricochet. Howell (1944) recognized essentially the same gaits but called the amble the running walk, the rack the pace, and the ricochet the bipedal hop. He also subdivided some of these groups and mentions the half-bound. Dagg (Zoc. cit.) combines canter, transverse gallop and rotary gallop in one group, the gallop, and, like Howell, prefers the terms pace and running walk. These last are the least ambiguous terms: the running walk is sometimes referred to as the rack, as well as the amble, while the pace is also termed either rack or amble in some books. Dagg introduces one extra term, the bound, recognizes the use of the tail as an additional support in slow walking of some species, and adds the bipedal walk, characteristic of humans, to the list of gaits.

This abundance of terms, not to mention the differences in usage between authors, suggest a complex situation which is more apparent than real. An individual animal, indeed an individual species, has generally only two or three gaits and there is no difficulty in distinguishing which of these it is using at any time. They may be, for instance, a walk (for slow movement), a trot, and a gallop (for fast movement), anything else appearing only as a short-lived transition between these. The difficulty in description comes when one attempts to compare the gaits of very different animals; the running walk of a lightweight horse may appear more like the trot of a carthorse than like the latter’s running walk. With totally different species


a verbal comparison becomes even more difficult. Hildebrand (1965) has devised thirty-nine terms just for variations of the slower, symmetrical, gaits; the forms of galloping and bounding would require additional terms.

In fact, some more mathematical approach to gait analysis is required, and this has been provided by Hildebrand (1965, 1966) and by Dagg & De Vos (1968a,b).

The gait of a mammal is made up of three components; the proportion of the stride which each limb spends on the ground, the sequence in which the limbs are moved, and the time taken to complete a stride. A cine film can be analysed into the percentage of the stride during which each foot, or combination of feet, is in use. This is the basis of the comparisons made by Dagg & De Vos (1968a,b). Hildebrand has carried the analysis further, in some respects, by expressing it in a neat, graphical manner. This is done by plotting just two variables, the percentage of the stride that each hindfoot spends on the ground, and the percentage of the stride that the front footfall of the same side lags behind it. Using this sort of approach we can define the basic gaits, but the limitations of these as descriptive terms need to be born in mind.

Walk A slow gait in which, ideally, each hindlimb spends 75 % of the stride on the ground and each forelimb follows 25% of the stride after the hindlimb of the same side. Only one foot, therefore, is in the air at a time and three limbs provide support.

Running walk A somewhat faster gait, with each hindlimb on the ground 50% of the time, and the fore foot 25% of the stride time behind it. Two feet may be in the air, and two in support, for most of the time.

Trot A faster gait, where each hindfoot spends only about 30% of the stride on the ground and the forelimb is 50% of the stride behind it. Support is therefore provided by diagonal pairs of limbs but is not continuous.

Pace A gait of similar speed to the trot, with the hindfoot on the ground for only 30% of the stride. However, the forelimb is, ideally, 0% of the stride behind it, so that support is provided alternately by pairs of ipsilateral (same side) limbs.

All of these are regular gaits, that is, the left side limbs repeat what the right side limbs have just done, half a stride later. The gallops are irregular gaits, with no such correspondence between the limb actions.

Rotary gallop The hindfeet only spend in total about 30 % of the stride on the ground in a gallop; this may theoretically be split 15 % between each foot or in any permutation. The forelimbs spend a similarly short, but irregular, period of time on the ground. For up to 50 % of the stride, the animal is in suspension, airborne. In a galloping horse there is only one period of suspension with all the limbs gathered up beneath the body (bunched suspension). In other animals there may also be a period of extended suspension as the animal leaps from its back legs. In a rotary gallop, the sequence of foot falls runs either ‘clockwise’ (right hind, left hind, left fore, right fore) or in the comparable ‘anticlockwise’ sequence.

Transverse gallop Support timings in this gait are, as in the rotary gallop, rather brief. The order of the footfall differs from the rotary gallop in being left hind, right hind, left fore, right fore or the comparable reverse sequence.

128 J . Clevedon Brown and D. W. Yalden

Bound A symmetrical gait with similar brief support periods to the gallops. However, the hindlimbs act as a synchronous pair of supports and so, after an extended suspension, do the front pair.

Half-bound The hindlimbs operate as a pair, just as in the bound, but the front limbs do not. The gait is therefore only partially symmetrical.

Ricochet The hindlimbs alone are used, as a synchronous pair of supports, resulting in the typical fast gait of saltatorial mammals such as kangaroos.

The gait describes the locomotion of the mammal as a whole, but it can also be very useful in describing and comparing movements within the limbs at particular joints. At its simplest this can be done by examining the extent of the articular facets on the bones or by manipulating fresh dead material (Yalden, 1970, 1971, 1972). However, this is not very satisfactory and a far better approach has been used by Jenkins (1970, 1971). By using cineradiography and analysing the movements a t the joints, he has presented an analysis of limb function in smaller mammals which was not previously available. An extension of this technique to other mammals, and perhaps to faster gaits, would yield interesting results. For larger mammals, the analysis of ordinary cine film (e.g. Hildebrand, 1959) can give similar results. Tuttle (1969) has obtained data of this sort for large primates by manipulating them under anaesthesia. The recent study by Goslow, Reinking & Stuart (1973) suggests that this approach may also be valuable in integrating locomotory studies and physiological studies, which we anticipate (Discussion, p. 132) as a necessary future step.

DISCUSSION Descriptive terms for limb variants and different forms of stance, and for different types of locomotor pattern are much used and have a real value for scientific communication but, overall, they seem to suffer from a lack of precise definition and can be misunderstood and misused. It is clear, too, that the studies on which they are based are still very incomplete, both within and between the mammalian orders. I t is impossible to review these studies in detail within this paper; many lengthy reviews would be needed. It is possible, quite briefly, to assess the various approaches to the study of mammalian limbs and locomotion, summarizing their strengths and limitations, determining how they relate to one another, and recognizing the gaps between them.

The great value of the comparative anatomical approach is the light thrown on evolutionary trends and processes and in highlighting evolutionary ‘novelties’ (Lewis, 1964) as subjects demanding study. Comparative anatomy is the basis for reconstructing palaeontological material and the broad basis on which living and fossil species are classified. However unfashionable currently, it is one of the most fundamental disciplines. It is, however, a discipline expressed mainly in static terms. It deals with parts and the parts, added together, do not make a whole living animal. As regards locomotory function, structure cannot be accurately interpreted beyond the grossest categories ; of stance, or as indicating specialization towards the climbing (scansorial), swimming (natatorial), burrowing (fossorial), or flying (volant) habits. Morphological indications of habits may be quite lacking, however. Lewis (1964) points out that the evident arboreal specializations of Primates must be due to adaptations beyond those needed for merely leaving the ground for the trees; opossums are arboreal, and possibly have been so since the Cretaceous, yet they are regarded as the most generalized of extant mammals. Morphological data alone can lead to quite erroneous functional interpretations. An interesting case is the study by Evans (1942) of the osteology of the Elephant shrews (Macroscelididae). The members of this family of African insectivores are commonly


believed to be ricochetal on the basis of early incomplete observations and circumstantial evidence. They are, in fact, quadrupedal (Brown, 1964) although at speed there are long phases in suspension. Evans was not biased by mistaken preconceptions since he had it on good (unpublished) authority that the species under study were quadrupedal. Nevertheless, his osteological analysis indicated that the family, as a whole, showed a strong tendency towards ricochetal adaptation. The adaptive features of the macroscelid limbs misleadingly parallel those expected of hopping ammals. Marlow’s (1969) comparison of the morphologically similar Antechinomys, which bounds, with Notomys, which ricochets, makes the same point.

Comparative myology or comparative morphology in the wide sense of including skeletal, muscular and joint elements, is less advanced than purely osteological studies. Even so the literature is immense. Much of this data, apart from continuing studies in veterinary anatomy, was published at about the turn of the century and included wide surveys as well as descriptive anatomical studies of individual species. Surveys, such as that of Windle (1894; 1896) on the myology of rodents, are essentially registers of the muscles present within the members of a taxonomic group, together with a subjective indication of the range of interspecific variation. Although incomplete, such registers are potentially very valuable but, unfortunately with work of this period there is always some doubt whether the samples used were sufficiently large enough to be representative. Researches since that date include excellent detailed anatomical descriptions of individual species and, most recently, comparative studies of particular regions of the limb. Studies on different regions of the limbs of Primates and comparative studies of the carpus and tarsus have already been mentioned. The papers of Lewis (1962, 1963, 1964) are particularly interesting in emphasizing the value of the foot as an adaptive structure and in throwing new light on evolutionary trends.

There are few studies which aim directly at correlating limb morphology with locomotory function. That of Reed (1951) on three soricoid insectivores is of particular interest within the terms of this discussion. He attempted to quantify differences between his study species by volumetric measurements of individual muscles. Quite apart from the technical difficulties of obtaining accurate measurements, this sort of approach is open to the criticism that muscle mass in itself is not a very meaningful parameter. More important properties are variations in the shape of the muscle, in its angle of action, and its proportional composition of red and white fibres. Moreover, muscles do not work in isolation but in different combinations and oppositions which may vary at different times or under differing conditions. The reduction of a muscle in one species as compared with another related species may be more than com- pensated for by synergistic effects or by increased leverage due to advantages of shape and insertion. Functional analysis in these terms calls for a sophisticated statistical approach, given that the technical difficulties of obtaining accurate raw data can be overcome.

The behavioural approach takes the living, active, animal as its study material but its study poses considerable technical difficulties. Cinematography was adopted early on (cf. Muybridge, 1899) as a means of accurately recording movement. This is an indispensible, though ex- pensive, technique requiring a high level of expertise with both the equipment and the subjects. Difficulties of descriptive language have already been discussed. Although Man is a pre- dominantly visual animal, what he sees is appreciated more in terms of size, shape, texture and colour. The atavistic response to movement is to identify the moving shape to determine its potential harmlessness or menace. The relative speed of movement might be important to man, e.g. as a hunter, but the details of movement are not, except in himself and the horse which he rides almost as an extension of himself. Language to describe gaits comparatively is not natural to us and must be defined accurately and. used accurately. Then there are difficulties in analysing the movements recorded. Every new field of study or discipline in biology proceeds in two phases; at the beginning there is the descriptive phase, in which phenomena are collected and described to become factual data, followed by the deductive phase in which the data is used to derive generalizations and hypotheses. The descriptive


phase in mammalian locomotory behaviour is still very incomplete. Nevertheless, important analytical and deductive exercises have been made. Gray (1944) reduced the phases of locomotory cycles to simple models, analogous with tables and stools, which could be analysed mathematically. This has led to valuable generalizations about physical factors in locomotion, particularly about movements of the centre of gravity, the effects of fricton, and the forces which must act about the points of support. The general theoretical principles derived can be applied to actual cases allowing, for instance, inferences to be made about integrated muscular actions at a joint. Hildebrand uses records of locomotory sequences for analyses in biomechanical terms. His studies are mainly of extreme cursorial forms in which movements of the body (the limbs, girdles and vertebral column) are marked. These studies enable close correlations to be made between morphology and function in cursorial mammals. The application of cineradiography (cf. Jenkins) holds great promise for the future. More data can be recorded and the method is particularly suitable for the smaller and more generalized mammals. A particularly important result of this application is the need to reconsider concepts about the generalized mammalian limb and what characterizes it compared with other vertebrate classes (Jenkins, 1971).

The morphological and behavioural approaches are clearly reaching out towards each other and there is an obvious case for conjoint studies. The real link between these two disciplines lies, however, in a third, quite separate, field of research. The limb, as a structure, functions through physiological mechanisms while locomotory behaviour can be regarded as an observable expression of integrated physiological activity. Physiological studies of locomotion also comprises a vast literature and, again, there are formidable technical difficulties involved in the investigations. Mammals lend themselves less readily to the experimental and operative techniques and greater progress has been made in studies of fish and amphibian locomotion. Essentially we are concerned with nerve-muscle physiology. Great progress has been made at the cellular level in investigating the transmission of the nerve impulse, the biochemistry of the motor end plate, and the contractile mechanism of the muscle fibre. Understanding of total nervous control and of the integration of muscle responses is far less certain. Proprio- ceptive reflexes are believed to play a fundamental role in vertebrate locomotion (Gray, 1950). These are local reflexes of the spinal cord which, nevertheless, can be responsible for quite complex patterns of movement. The timing of these is clearly a function of higher centres in the brain. The mammalian brain, as a result of transection, stimulation, and other experimental procedures, is found to have several centres controlling motor function but at varying levels of complexity. This hierarchy of control parallels the sequential development of total correlation centres during the phylogeny of the vertebrate brain and these also fall into a hierarchical sequence. In fish and amphibians total correlation is centred in the midbrain roof (optic tectum). The midbrain floor is the anterior end of the segmental nervous system and the motor centres here have a general control over all those of the spinal cord. Also, in conjunction with the vestibular centres of the hindbrain and the palaeocerebellum, these centres are responsible for the maintenance of posture-complex, but stereotyped reflexes of which the postural and righting reflexes are examples. In diapsid reptiles and the birds, total correlation is shifted forward to the thalamic and striatal regions of the forebrain, the midbrain roof remaining as a subordinate correlation centre. Instead of one computational centre there are now two, linked, centres. The new one carries out correlations of all kinds of sensory information received both directly and, indirectly, as ready correlated information from the midbrain. Obviously there are greater opportunities for increasing neuronal interconnections and for increasing behavioural patterns. With the development of association pathways there develops some capacity for learning. The thalamico-striatal region of mammals is known to have an important role in the control of motor functions but this is poorly understood. This is hardly surprising considering the complexity of the region and the close interconnections of so many different modalities. For instance, stimulation of certain areas of the hypothalamus, a visceral area, will produce somatic motor reactions such as persistent walking. Such results


indicate the close and complex interactions of the different centres and pathways of the forebrain. In mammals the thalamico-striatal correlation centre is in turn dominated by a third development of a total correlation centre-the cerebral cortex. The cortex has an enormous capacity for growth in absolute size and in the number of neuronal connections. The motor cortex of mammals ultimately controls motor function both directly, by way of new pathways including connections with the neocerebellum, and indirectly, by way of the phylogenetically older correlation centres and their pathways. The neocerebellum (cerebellar hemispheres) is a mammalian development with functions directly related to fine muscular control. One of the consequences of cortical control is the capacity for correlations with stored information-memory-with greater possibilities for learning and, in some cases, inventing, by a deliberate and conscious effort, new patterns of behaviour.

These higher centres are concerned with computational processes and with programming appropriate body responses. Control of motor activity, including locomotion, is clearly very complex in mammals and there should be a great potential for flexibility in responses. The extent to which this potential can be realized depends, firstly, on the biomechanical limitations of the effector structures and, secondly, on the availability of suitable neuronal pathways between the control centres and the effectors. In general, the limbs of mammals are structurally more differentiated and functionally more flexible than those of other vertebrates and they are capable of the wide range of individual movements which we roughly classify into retraction, protraction, adduction, abduction, supination and pronation. Movement of the amphibian limb is reflex and the muscles are activated in an invariable, ordered, sequence to produce the locomotory movement. All the available evidence indicates that nerve-muscle effector systems are precisely ordered patterns. The nervous impulse itself is invariable; neurons operate on the all-or-none principle. Ordering and variations of the system can be achieved by inhibitory pathways and by the variable resistance to transmission of the impulse at the synapses and nerve-effector junctions. Local and brainstem reflex pathways are established, invariable, neuronal circuits in which synaptic resistances are minimal. Once an adequate stimulus is applied the response follows, rapidly, automatically and unconsciously. Reflexes of this sort are believed to be phylogenetically old and to be genetically determined. At the other extreme, are pathways established by the mammals’ capacity for learning. A programme for a new pattern of motor activity will, at first, be executed tentatively and hesitantly. Practice or training is needed to perfect the action. This depends on facilitation- the phenomenon whereby resistance at the synapses along a neuronal sequence is weakened by repeated use of the pathway. In this way, the overall response to that pathway becomes progressively more rapid and automatic, although control remains conscious. These are two extremes of a graded sequence in the development of neuronal pathways. Somewhere in between are the innate behaviour patterns typical of thalamus dominated vertebrates. These patterns are to some degree genetically assimilated and, while they are facilitated reflex pathways, they are not necessarily invariable. In mammalian locomotion, neuronal pathways of all degrees are involved. Spinal and midbrain reflexes are essential for posture, innate patterns determine the basic, infantile, progression, but full control of the locomotory repertoire has to be individually learnt. The evolution of neuronal pathways is quite as important to locomotion as evolution of limb morphology.

In biological research it is a common, and rewarding, practice to commence the study of a feature of interest in those species in which the feature is specialized or hypertrophied. The results can then be used to extend the study to more generalized species in which the feature of interest is more cryptic and difficult to observe. So far, in the study of mammalian locomotion, the more generalized species have been largely neglected, while the study of more specialized species is tending to distort conceptual thinking on the subject. It is apposite to mention, again, Jenkins’ (1971) criticism of the accepted definition of what characterizes the mammalian limb. Some brief considerations of more generalized mammals may serve to indicate that their study is overdue. Mammals may have specialized life habits without


evident morphological adaptations, in general, or in the limbs, in particular. The opossum has already been mentioned as an ideal generalized, yet arboreal, mammal. Many mammals are fossorial without limb modifications. Most terrestrial mammals can climb and swim at need, are capable of a variety of gaits, and have a variety of non-locomotory limb functions. The biomechanics of the extreme unguligrade limb may possibly appeal to us because it is more akin to precision engineering. In this respect it is a simplification of the mammalian limb which functions generally on complex homeostatic principles which combine flexibility and precision of movement with wide tolerances and margins of safety ; functional patterns can be adapted without the need for morphological changes. Closely related species, for instance, Rattus rattus and R . norvegicus, can be indistinguishable in limb morphology and yet have distinctive locomotory habits. Studies of the bony pelvis of rodents (Brown & Twigg, 1969) and of pelvic myology (unpublished studies) suggest, in fact, that intraspecific variation is of a greater degree than interspecific variation and cannot be correlated with differences in locomotor behaviour. Such variation, and also quite extensive injury, can be absorbed without disfunction.

Osteo-archaeologists interested in the origins of animal husbandry have recently questioned the validity of morphological criteria for recognizing domestication. Some have gone further and posed the real question; that the domestic habit must have been established before selection, witting or unwitting, had produced evident morphological variation. This sums up, from a completely different standpoint and in miniature form, the conclusions to be reached from this discussion. We would propose that changes in limb morphology, sufficiently distinctive to be of taxonomic value, can only become evident at the end of an evolutionary sequence and as a result of complex, multiple, adaptive pressures, rather than simple shifts of life habit (Lewis, 1964). Such an evolutionary sequence provides a conceptual framework for synthesizing the results of the several different approaches to the study of mammalian locomotion. In an idealized form, the sequence is as follows: Ecological changes may lead to changes in locomotory behaviour or the reinforcement of behavioural tendencies. If the pressure persists, the change may become irreversible with the establishment of a new behavioural pattern (Behavioural studies). If the new behaviour pattern is maintained without modification, facilitated neuronal pathways for particular patterns of muscular co-ordination may become genetically assimilated (Studies in neuromuscular physiology). If the new pattern of behaviour involves a divergence in muscular co-ordination, then, through the law of use and disuse, changes in the myology of the limb may become established with more or less concomitant osteological changes (Anatomical studies).

Certainly the study of mammalian locomotion is an involved and difficult field but this need not deny the participation of the ordinary mammalogist lacking equipment and training in specialized research disciplines; there is a very real need for expanded investigations at the behavioural level and many of these require only a relatively simple investigative approach. For example, we mentioned differences in the locomotory behaviour of Rattus rattus and R. norvegicus. A comparative study of these two species, under field conditions, to determine just how scansorial or terrestrial they are, has not been carried out. As another example, a comparison of the gaits of mice (Apodemus, Mus) and voles (Clethrionomys, Microtus) could begin with a quantitative study of their tracks recorded on sooty paper (Justice, 1961 ; Bailey, 1969). The list of possible simple investigations is endless.

REFERENCES ASHLIY, K. R. (1972) Patterns of daily activity in mammals. Mammal Review, 1, 171-185. ASHTON, E. H. & OXNARD, C. E. (1964) Functional adaptations of the primate shoulder girdle. Proceedings of

BADOUX, D. M. (1965) Some notes on the functional anatomy of Macropusgiganteus Zirnm. with general remarks

BAILEY, G. N. A. (1969) A device for tracking small mammals. Journal ofZoology, London, 159,513-540. BEDDARD, F. E. (1902) Observations upon the carpal vibrissae in mammals. Proceedings of the Zoological

the Zoological Society of London, 142,49-66.

on the mechanics of bipedal leaping. Acta Anatomica, 62,418-433.

Society of London, 1902, 127-136.

Limbs and locomotion of terrestrial mammals I33

BOESSNECK, J. (1969) Osteological differences between sheep (Ovis aries Linnk) and goat (Capra hircus LinnC). I n : Science in Archaeology Brothwell, D. & Higgs, E. S . (eds). 2nd edn. Thames & Hudson, London.

B ~ K ~ N Y I , S. (1969) Archaeological problems and methods of recognizing animal domestication. In: Ucko & Dimbleby (eds) op. cit.

BROWN, J. C. (1964) Observations on the Elephant shrews of equatorial Africa. Proceedings of the Zoological Society of London, 143, 103-1 19.

BROWN, J. C. (1971) The description of mammals. 1. The external characters of the head. Mammal Review,

BROWN, J. C. & TWIGG, G. I. (1969) Studies on the pelvis of British Muridae and Cricetidae (Rodentia). Journal of Zoology, London, 158, 81-132.

CHAPLIN, R. E. (1969) The use of non-morphological criteria in the study of domestication from bones found in archaeological sites. In: Ucko & Dimbleby (eds) op. cit.

CLARK, W. E. LEGROS (1936) The problem of the claw in Primates. Proceedings of the Zoological Society of London, 1936, 1-24.

CLEMENS, W. A. (1970) Mesozoic mammalian evolution. Annual Review of Ecology and Systematics, 1,357-390. CORNWALL, I. W. (1956) Bones for the archaeologist. Phoenix, London. Cox, C. B. (1967) Changes in terrestrial vertebrate faunas during the Mesozoic. In: The Fossil Record. Harland,

W. D. et a/. (eds). Pp. 77-89. The Geological Society, London. DAGG, A. I. & DE Vos, A. (1968a) The walking gaits of some species of Pecora. Journal of Zoology, London,

DAGG, A. I. & DE Vos, A. (196813) Fast gaits of pecoran species. Journal of Zoology, London, 155,499-506. EVANS, F . G. (1942) The osteology and relationships of the Elephant shrews (Macroscelididae). Bulletin of the

EWER, R. F. (1973) The Carnivores. Weidenfeld & Nicholson, London. FLOWER, W. H. (1870) An Introduction to the Osteology of the Mammalia. Macmillan, London. GOSLOW, G. E., REINKING, R. M. &STUART, D. G. (1973) The cat step cycle: hind limb joint angles and muscle

GRASSE, P. P. (ed.) (1955) Trait6 de Zoologie. 16. MammifPres; les Ordres: Anatomie, Ethologie, Systematique.

GRASSE, P. P. (ed.) (1967) Trait6 de Zoologie. 17, part I . Mammiferes. Tkguments. Squellette. Masson, Paris. GRAY, J. (1944) Studies in the mechanics of the tetrapod skeleton. Journalof Experimental Biology, 20,88-116. GRAY, J. (1950) The role of peripheral sense organs during locomotion inthe vertebrates. Symposia of the

GREGORY, W. K. (1912) Notes on the principles of quadrupedal locomotion. Annals of the New York Academy

GREGORY, W. K. (1937) The bridge-that-walks. Natural History, New York, 39, 33-48. HAINES, R. W. (1958) Arboreal or terrestrial ancestry of placental mammals. Quarterly Review of Biology, 33,

HALL-CRAGGS, E. C. B. (1965) An analysis of the jump of the Lesser galago (Galago senegalensis). Journalof

HERRE, W. (1969) The science and history of domestic animals. In: Science in Archaeology. Brothwell, D. &

HIGGS, E. S. (ed.) (1972) Papers in Economic Prehistory. The University Press, Cambridge. HIGGS, E. S. & JARMAN, M. R. (1972) The origins of animal and plant husbandry. In: Higgs, E. S. (ed.) op. cit. HIGHAM, C. & MESSAGE, M. (1969) An assessment of a prehistoric technique of bovine husbandry. In: Science

HILDEBRAND, M. (1959) Motions of the running cheetah and horse. Journal of Mammalogy, 40,481-495. HILDEBRAND, M. (1960) How animals run. Scientific American, 202, 148-157. HILDEBRAND, M. (1965) Symmetrical gaits of horses. Science, New York, 150, 701-708. HILDEBRAND, M. (1966) Analysis of the symmetrical gaits of tetrapods. Folia Eiotheoretica, 6, 9-22. HILL, W. C. 0. (1954 et seq.) Primates. Comparative Anatomy and Taxonomy. Vol. 1-in continuation. Univer-

sity Press, Edinburgh. HILL, W. C. 0. (1955) Primates, Comparative Anatomy and Taxonomy. Vol. 2. Haplorhini: Tarsioidea.

University Press, Edinburgh. HODGSON, G. W. I. (1968) A comparative account of the animal remains from Corstopitum and the Iron Age

site of Catcote, near Hartlepools. County Durham. Archaeologia Aeliana, 4th series, 46, 127-1 62. HOFMANN, P. R. (1966) Field and laboratory methods for research into the anatomy of East African game

animals. East African Wildlye Journal, 4, 115-138. HOWELL, A. B. (1937) The swimming mechanism of the platypus. Journal of Mammalogy, 18,217-222. HOWELL, A. B. (1944) Speed In Animals. University Press, Chicago. HUE, E. (1907) Musk, Ost6olgique, Etude de la Faune Quaternaire. Ost6ometrie des MammifPres. Reinwald-

JARMAN, M. R. & WILKINSON, P. F. (1972) Criteria of animal domestication. In: Higgs, E. S . (ed.) op. cit. JENKINS, F. A. (1970) Limb movements in a monotreme (Tachyglossus aculeatus): a cineradiographic analysis.

JENKINS, F. A. (1971) Limb posture and locomotion in the Virginia opossum (Didelphis marsupialis) and in

JONES, F. W. (1923) The Mammals of South Australia, Part 1. Government Printer, Adelaide. JUSTICE, K. E. (1961) A new method for measuring home ranges of small mammals. Journal of Mammalogy,

KURT~N, B. (1968) Pleistocene Mammals of Europe. Weidenfeld & Nicholson, London.

1, 151-168.

155, 103-110.

American Museum of Natural History, 80, 85-1 25.

lengths during unrestrained locomotion. Journal of Morphology, 141, 1-42.

Masson, Paris.

Society for Experimental Biology, Cambridge, 4, 1 12-1 26.

of Sciences, 22,267-294.

1-23.

Zoology, London, 147,20-29.

Higgs, E. S. (eds). Thames and Hudson, London.

in Archaeology. Brothwell, D. & Higgs, E. S . (eds). 2nd edn. Thames & Hudson, London.

Schleicher, Paris.

Science, New York, 168, 1473-1475.

other non-cursorial mammals. Journal of Zoology, London, 165,303-3 15.

42,462470.

134 J. Cleveland Brown and D. W. Yalden

LEWIS, 0. J. (1962) The phylogeny of the crural and pedal flexor musculature. Proceedings of the Zoological

LEWIS, 0. J. (1963) The monotreme cruro-pedal flexor musculature. Journal of Anatomy, London, 97, 55-63. LEWIS. 0. J. (1964a) The evolution of the long flexor muscles of the lea and foot. International Review o f

Society of London, 138, 77-109.

General and Experimental Zoology, 1, 165-3 85. LEWIS, 0. J. (1965) Evolutionary changes in the primate wrist and inferior radio-ulnar joints. Anatomical

Record, 151,275-286. LEWIS, 0. J. (1972) Osteological features characterizing the wrists of monkeys and apes, with a reconsideration

of this region in Dryopithecus (Proconsul) afiicanus. American Journal of Physical Anthropology, 36,45-58. MARLOW, B. J. (1969) A comparison of two desert-living Australian mammals, Antechinomys spenceri (Mar-

supialia: Dasyundae) and Notomys cervinus (Rodentia: Muridae). Journal of Zoology, London, 157, 1 59-1 67

-

- - - - - . . MWBRIDGE, E. (1899/1957) Animals in Motion. Reprint; New York, Dover. NEAL, E. (1948) The Badger. Collins, London. OXNARD, C. E. (1968a) A note on the fragmentary Sterkfontein scapula. American Journal of Physical Anthro-

OXNARD, C. E. (1968b) A note on the Olduvai clavicular fragment. American Journal of Physical Anthropology,

OXNARD, C. E. (1968~) Primate evolution-a method of investigation. American Journal of Physical Anthro-

OXNARD, C. E. (1969) Evolution of the human shoulder: some possible pathways. American Journalof Physical

OXNARD, C. E. & NEELY, P. M. (1969) The descriptive use of neighbourhood limited classification in functional

PAYNE, S. (1972) On the interpretation of bone samples from archaeological sites. In: Higgs, E. S. (ed.) op. cit. POCOCK, R. I. (1910) On the specialised cutaneous glands of ruminants. Proceedings of the Zoological Society

POCOCK, R. I. (1914) On the feet and other external features of the Canidae and Ursidae. Proceedings of the

POCOCK, R. I. (1925) The external features of the Lagomorpha. Proceedings of the Zoological Society of London,

REED, C . A. (1951) Locomotion and appendicular anatomy in three soricoid insectivores. American Midland

REED, C. A. (1963) Osteo-archaeology. In: Science in archaeology. Brothwell D. & Higgs, E. S. (eds). 1st edn.

pology, 28,213-218.

29,429432.

pology, 28,289-302.

Anthropology, 30, 319-332.

morphology: an analysis of the shoulder in Primates. Journal of Morphology, 129, 127-148.

of London, 1910, 840-986.

Zoological Society of London, 1914, 913-941.

1925,669-700.

Naturalist, 45, 5 13-671.

Thames & Hudson. London. ROBINSON, P. L. (1971)' A problem of faunal replacement on Permo-Triassic continents. Palaeontology, 14,

ROMER, A. S. (1966) Vertebrate Paleontology. 3rd edn. University Press, Chicago. RYDER, M. L. (1969) Animal Bones in Archaeology. Blackwells, Oxford. SAUNDERS, J. T. & MANTON, S. M. (1969) A Manual of Practical Vertebrate Morphology. 4th edn., revised

SCHAEFFER, B. (1947) Notes on the origin and function of the Artiodactyl astragalus. American Museum

SCHMID, E. (1 972) Atlas of Animal Bonesfor Prehistorians, Archaeologists and Quaternary Geologists. Elsevier,

SIMPSON, G. G. (1945) The principles of classification and a classification of the mammals. Bul/etin of the

SLIJPER, E. J. (1961) Locomotion and locomotory organs in whales and dolphins (Cetacea). Symposia of the

SMITH, J. M. & SAVAGE, R. J. G. (1956) Some locomotory adaptations in mammals. Journal of the Linnean

TUITLE, R. H. (1969) Quantitative and functional studies on the handsof the Anthropoidea. 1. The Hominoidea.

UCKO, P. J. & DIMBLEBY, G. W. (eds) (1969) The Domestication and Exploitation of Plants and Animals.

131-1 53.

S. M. Manton & M. E. Brown. Clarendon Press, Oxford.

Novitates, 1356.

Amsterdam.

American Museum of Natural History, 85, 1-350.

Zoological Society of London, 5, 77-94.

Society of London, Zoology, 42,603-622.

Journal of Morphology, 128, 309-364.

Duckworth, London.

the Zooloaical Societv of London. 1894.251-295. WINDLE, F. G. (1894) On the myology of the sciuromorphine and hystricomorphine rodents. Proceedings of

WINDLE, F. GI (1896) MiolGgy of rodents.' 11. An account of the myology of the Myomorpha, together with a comparison of the muscles of the various suborders of rodents. Proceedings of the Zoological Society ofLondon, 1896, 159-192.

WEBER, M. (1927) Die Saugetiere. I. Anatomisches Teil. 2nd edn. Fischer Verlag, Jena. YALDEN, D. W. (1966) The anatomy of mole locomotion. Journal of Zoology, London, 149, 55-64. YALDEN, D. W. (1970) The functional morphology of the carpal bones in carnivores. Acra Anatomica, 77,

YALDEN, D. W. (1971) The functional morphology of the carpus in ungulate mammals. Acta Anatomica, 78,

YALDEN, D. W. (1972) The form and function of the carpal bones in some arboreally adapted mammals.

ZEUNER, F. E. (1963) A History of Domesticated Animals. Hutchinson, London.

481-500.

461-487.

Acta Anatomica, 82, 383-406.

the description of mammals–2 limbs and locomotion of terrestial mammals

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