Introduction
The idea that mobility of upper limbs was least in prosimians, greater in monkeys, greater still in apes, and most in humans was a useful idea for viewing the primates in earlier times. But new information and ideas about primate locomotion now reveal that upper limb function is better described in other ways.
The underlying difference between basically arboreal primates and terrestrial mammals: that is, in comparison to compressive forces in the forelimbs of terrestrial mammals, tension-bearing by upper limbs is a phenomenon of most activities that primates undertake. Thus, though tension-bearing is most easily seen in brachiation and arm-swinging, as practiced by some apes and monkeys, it is also a part of most locomotor actions that involve upper limb raising, body support from above, climbing, and other acrobatic movements, together with a wide variety of foraging and other activities only marginally within the concept of locomotion.
Individual primates are less characterized by specific activities than they are by the amazing mix of activities, different in different primates, which they undertake. Thus, though all primates can do almost all things, the mix producing variable degrees of tension-bearing, is what distinguishes the various species from each other.
It is perhaps also worth asking questions about locomotion in higher primates. Much attention has been paid to this in recent years so that leaping is well documented, for instance, as a major mode of locomotion.
When we consider leaping in those other primates not usually thought of as leaping animals at all, we see mid-air positions in which limbs cycle or even wave wildly; it appears at first sight as though no good biomechanical mechanisms are at work at all. Thus, curious mid-air positions are found in forms such as macaques, mangabeys, gibbons, and spider monkeys. And the most unlikely mid-air positions of all are found in the most unlikely leapers of all, such species as spider monkeys, gibbons, and siamangs.
Most naturalistic studies of primates did not begin until 1960; studies of the mode of locomotion began in 1967. Thus, information on the interrelationships of morphology, locomotion, and use of habitat is still incomplete.
The Body of the paper
The Grades of primate evolution
Organismic studies suggest a linear arrangement of grades of primates from prosimians, through various monkeys, to apes and humans.
The Lemuroids
Primates have been traditionally considered to be closely related descendants of an early insectivore stock lumped Dermoptera (colugos, e.g., flying lemurs), Chiroptera (bats), Primates, and Menotyphla (e.g., tree shrews) into one monophyletic superordinal group, the Archon. He included tupaiids (tree shrews) with primates and other archons because he believed the skull structure of tupaiids was like lemuroids and different from insectivorous.
Whether of limb girdles, limb segments, whole limbs, or overall bodily proportions) some representatives of genera from each morphological mode are analyzed, in no single study are all genera represented.
For instance, for the shoulder girdle, information is presented for only one indriid form: the sifaka. For the pelvic girdle, there are data for both sifakas and indris. In both shoulder and pelvic studies, regular and needle-nailed bush-babies alone represent what is subsequently discovered to be a mode including all bush-babies and tarsiers. It is only in the investigations of the limbs as a whole and of overall bodily proportions that data for tarsiers is included. And it is only in the limb and overall bodily proportion studies that avahis are represented and found to lie with indris and sifakas.
Lemur, ring-tailed
Ring-tailed lemurs, mongoose lemurs, black lemurs, and ruffed lemurs are also reasonably able leapers though they are also more quadrupedal than, for instance, the indriids and the galaxies. Of the various lemur species, L. variegatus leaps to perhaps the least degree of all, it is said to be quite clumsy in the trees.
It thus seems clear that we now have at least three morphological adaptations for leaping, in addition to the leaping superimposed upon the quadrupedalism of most Lemur species. We are thus left with a series of possibilities that complicate and extend those already mentioned briefly.
Even when we come to study prosimians, such differences can be found. Those prosimians that are most nearly regular quadrupeds with the most pronograde bodily habits do the various things leading to tension-bearing in raised positions to the least degrees, although even in this group these tension-bearing activities do occur because all move in the small-branch habitat for at least part of the time.
And in the indriids, though their locomotion is characterized by long leaps, the various ancillary movements of which their upper limbs are especially capable (certainly more so than for most other prosimians) make it clear that they too bear tensile forces and have raised upper limbs more than do most other primates.
Greater Bushbaby
Most studies of vertebrate locomotion have been carried out on animals other than primates. But because there have evolved among the primates several creatures highly adapted for leaping, there are a few excellent studies of leaping in which various primates are the subject materials.
Studies provide fascinating information totally unreachable save through the mechanisms of the technology. For instance, Hall Craggs ( 1965a, b) shows that the force developed in the limb applied to the ground is in the region of the tarsometatarsal joint and not at the distal ends of the metatarsal bones as has been assumed by most of the prior workers who depended upon anatomy alone and who did not have slow-motion photography.
The Tarsiers
Tarsiers are close to bush-babies, and aye-ayes are not close to indriids. In these two cases, the sizes of our samples are quite large so that this result is robust. Surely the results for these two particular groups are the evidence that denies our new hypothesis. It is, therefore, essential to look at these two cases in more detail.
There seems no problem about the lineage of Tarsius: a clear fossil record goes back through the Miocene to the Palaeocene, with the main belly of the radiation is in the Eocene. It is, of course, the case that almost all of this exotic fossil history is based upon dental characteristics; a good deal less depends upon other cranial features; the postcranial skeleton is scarcely known at all.
Yet this little animal, easily held in the palm of the hand, has for many years attracted the attention of comparative anatomists because it combines, in its anatomical organization, a number of remarkably basic characters together with an equally remarkable number of curious and highly specialized features.
The modern tarsier is a crepuscular and almost entirely arboreal creature. It shows marked specializations in the relatively enormous size of the eyes and in the peculiar modifications of the limbs for leaping among the branches. The ears are huge; the structure of the nose and upper lip resembles that of New World monkeys; the tail is large and long with epidermal ridges but is not prehensile in the usual sense of the term.
Horsfield’s tarsier has large eyes and large ears that are mobile. The Horsfield’s tarsier has a special adaptation in its neck and it can turn its head 180 degrees. Horsfield’s tarsier has two claws on each foot. The pelage color of this species is ivory yellow in Sumatra and golden brown. It is a vertical clinger and leaper. The elongated tarsus helps them in leaping.
Philippine tarsier is different from other animals and considered as the world’s smallest primate, it measures only about twelve centimeters in length. Normally it has a gray or brown pelage.
This species is a vertical clinger and leaper. This species also moves by hopping, quadrupedalism,
Spectral tarsier has large eyes and large ears that are mobile. It is a vertical clinger and leaper. It has elongated tarsus that helps them in leaping. This species also moves by climbing, hopping, or a slow quadrupedal type movement.
The Monkeys (New and Old)
New World
Upper limbs may be used during changes between locomotor activities to support, steady, and secure the body from above. This is found most markedly in all of the species mentioned above, but it occurs frequently in some New and Old World monkeys such as capuchins and howler monkeys, colobus monkeys, and langurs. And it is certainly not unknown in many of the other primates that live in the small-branch milieu
It is now also well-documented that upper limbs may be used in modes involving tensile forces and raised positions when animals suspend themselves momentarily, often prior to a downward drop. This, again, can occur in any primate. But those that are most quadrupedal and most terrestrial are least likely to do it. And it is again especially documented as being used by uakari monkeys, capuchins, howler monkeys, woolly monkeys, spider monkeys, and woolly spider monkeys of the New World, by colobus monkeys, langurs, and other colonies of the Old World, and especially by the indriids among the prosimians. Of course, it goes without saying that such activities form a part of the spectrum of actions of all apes.
Tensile-bearing activities also include propulsive actions of upper limbs in the rather special vertical climbing modes that can be adopted by all primates. Such vertical climbing can be done in a number of ways. One involves climbing upwards (or downwards) using alternate movements of limbs similar to regular quadrupedal movement. Another involves simultaneous movements of pairs of limbs as in ‘inch worming. But, because the upper limbs are above the center of gravity, all such vertical climbing modes imply the existence of tensile forces together with some degree of elevation. Activities such as these are also found in any primate on occasion. But they are undoubtedly more frequently noted in particular groups such as indriids and lorises, uakaris and saki monkeys, capuchins and howler monkeys, colobus and langurs, and, of course, all species capable of the more arm-swinging activities, the dateline New World monkeys and the lesser and greater apes.
As we view the various New World monkeys we can identify similar upper limb activities. It is well documented that the various lines possess tension-bearing facilities and raised upper limb positions to large degrees. Of the lines, the woolly monkey is the one least so endowed. But there is still no difficulty documenting that even this species does these things to very considerable degrees.
The anatomical similarity between howler monkeys and datelines was recognized early so that a degree of similarity in tension-bearing and raised positions in upper limbs was assumed. But some of the earlier studies examined the activities of howler monkeys in milieux where they could be easily viewed — not, in the case of the langurs, because they were upon the ground, but for a somewhat similar reason, that they were clearly visible upon open and relatively large branches. Such an environment militates against the more acrobatic activities predicted by the anatomy, and that might have been seen had the animals been studied in a smaller-branch milieu. In contrast, more recent investigations examine the movements of the animals in the close-branch environment; this allows the animals more scope for acrobatic movements.
Tamarin, golden lion is a small, squirrel-sized monkey with a long golden lion-like mane. Its diet consists of fruits, insects, and small lizards. They use fingers for probing into the cracks in the bark where they often find their food.
Red Uakari possesses a locomotor function and possesses abilities to suspend the body in part or even totally by the lower limbs. This too may be carried out in different ways, e.g. the lower limb suspension of some lorises when passing under branches is different from that of uakari monkeys when utilizing lower limb suspension in foraging.
Pale-headed is about 3.1 kilograms, and for the female, it is about 2.5 kilograms The color of the hair is black except for the nose that has white colored hair. It moves through the forest canopy quadrupedally. This species uses hindlimb suspension when feeding
When we come to the howler monkey that there are problems somewhat similar to those with the colobines. It is entirely possible that the problems stem in part from somewhat similar historical causes. The anatomical similarity between howler monkeys and datelines was recognized early so that a degree of similarity in tension-bearing and raised positions in upper limbs was assumed.
Old World
Monkeys Old World
In the relationship between brain size and body size, the primates are linearly arranged from New World monkeys, through Old World monkeys, to apes and humans. It is now also well-documented that upper limbs may be used in modes involving tensile forces and raised positions when animals suspend themselves momentarily, often prior to a downward drop. This, again, can occur in any primate. But those that are most quadrupedal and most terrestrial are least likely to do it. And it is again especially documented as being used by uakari monkeys, capuchins, howler monkeys, woolly monkeys, spider monkeys, and woolly spider monkeys of the New World, by colobus monkeys, langurs, and other colonies of the Old World, and especially by the indriids among the prosimians.
Many other actions are also related to the bearing of tension in upper limbs, and, to lesser degrees, to the propensity for raised positions. These include body-lifting actions of limbs in raising the trunk onto higher ledges or branches. This is obviously rather more frequent in those species whose environments more freely offer such ledges and branches.
It is well known that these animals hang before drops more than do most Old World monkeys. Lifting actions are particularly conspicuous in colobus monkeys especially when they are in the small-branch milieu. Pulling actions also occur not infrequently. Though Tuttle never saw colobus monkeys hanging by their upper limbs while feeding, he documents very well how they pull in, with the upper limbs, foods on springy branches well above their heads while sitting atop the larger boughs. And it is also well documented that, during feeding, colobus monkeys frequently employ their hands above their heads to steady themselves with grips on overhanging limbs. Such modes are less common in the cercopithecine monkeys whose propensities for full shoulder abduction and full elbow extension are considerably less.
There is a second cluster of New World genera. These species are known to be fairly highly acrobatic in their different ways and to occupy, compared to body size, a smaller-branch milieu. The spider and woolly spider monkeys (Ateles and Brachyteles) are exempted from this study on the grounds that they probably really are more comparable with the extreme brachiating primates, gibbons, and siamangs. There could even be a good reason for eliminating the woolly monkey on this basis; however, it is considerably more quadrupedal than Ateles and Brachyteles and approximates more to the quadrupedality of the howler monkey.
Those Old and New World monkeys that are generally regarded as quadrupedal are located in three groups each, and each of the three groups comprises genera that can be assigned as least acrobatic. This display is, of course, somewhat artificial because the various species, even those within the same cluster, can be statistically differentiated from each other. But there is an overall reality to the descriptions. And in the display of the morphological similarities within the clusters, taxonomic effects have been overcome because each cluster combines species from several taxonomic groups.
The Apes and Man
Biomechanics can be studied at a relatively simple level. It is easy to see, for instance, that the physical principles relating to size, load, and properties of materials provide considerable constraints that determine some of the limits of biological form. As a result, it has long been known that land animals constructed of conventional biological materials cannot exist above a certain size.
Electromyography has suggested that considerable forces may be borne by anatomical structures even when muscles are electrically silent ( Basma Jian, 1967). This particularly emphasizes the importance of knowing about a generally much-neglected topic, the existence of tension in biological structures, and the study, therefore, of ligaments and joint capsules. In turn, this provides new information about the workings of the limbs of fossil creatures.
Experimental stress analysis utilizing strain gauges in vivo has demonstrated, as a yet further illustration, that not only does the vertebral column help bear the obvious loads associated with posture and locomotion, but that each individual vertebra expands and contracts like a concertina as a result of hitherto generally neglected and apparently small cyclical forces such as those of the heartbeat and respiratory rhythm ( Lanyon, 1971, 1972 and 1973 ). This new finding, too, may have an impact on the study of fossil vertebrae.
Many types of research can be cited that today are providing new information about functional structural relationships in living species, and that, by analogy, may provide estimates about fossil forms. Thus, for instance, though we have no immediate extant biological equivalents in living species for the ‘sails’ of pelycosaurs or the ‘crests’ of hadrosaurs for studying their functions experimentally, in the case of many of the problems relating to human and primate evolution, reasonable inferences may indeed be made from models provided by the study of closely related living species.
The models may be entirely theoretical. For example, utilizing theoretical stress analysis of both living and fossil species, it has been suggested that the forms of some hand bones in dryopithecine apes are well adapted to use in palmigrade postures and gaits. Models of digitigrade locomotion in these fossils, as in some terrestrial monkeys today, or of knuckle-walking locomotion as in the terrestrial living African great apes, would appear to lead to greater stresses than are efficient in portions of the fossil bones. This indicates the unlikelihood of digitigrade or knuckle-walking locomotor patterns in these particular dryopithecine apes; it implies that these fossil apes were arboreal rather than terrestrial ( Preuschoft, 1973 ).
In a similar way, experimental stress-modeling has been applied to fossil shapes in comparison with the structures of extant species, the functions of which are known. It has been shown that the complicated architecture of the finger bones in the living apes relates fairly well to primary functions during locomotion and foraging, whether of the terrestrial knuckle-walking African apes, the gorilla, and chimpanzee, or whether of the arboreal, hanging-climbing Asian great ape, the orang-utan. A fossil finger bone from Olduvai has been shown, in related comparisons, to be mechanically more efficient in the arboreal mode than the terrestrial and to be nothing like that of man ( Oxnard, 1973a ). Similar arguments would seem to apply to all of the fossil hand bones (from both Olduvai and Hadar) that display the kinds of curvatures found in that finger bone.
In summary, then, those Old and New World monkeys that are generally regarded as quadrupedal are located in three groups each; and each of the three groups comprises genera that can be assigned as least acrobatic: ‘A’; more acrobatic: ‘B’; and most acrobatic: ‘C’ — even though the ‘A’s, ‘B’s and ‘C’s are different in the Old World monkeys than in the New. This display is, of course, somewhat artificial because the various species, even those within the same cluster, can be statistically differentiated from each other. But there is an overall reality to the descriptions.
The foregoing results of multivariate morphometric studies of australopithecines are the following: in terms of morphology, the various australopithecines are generally more similar to one another than any individual specimen is to any living primate. They are different from any living form to a degree greater than the differences between bipedal humans and terrestrial apes. Some of their similarities to living forms are especially reminiscent of the arboreal habitat.
The meaning of this is far more difficult to disentangle. It undoubtedly does not rest upon genetic propinquity as it is surely clear that, genetically, humans, the African apes, and presumably.
With each grade, begin by describing some general background and introductory information on that category of primate. Next, devote the remaining discussion of each grade to primate locomotion and body configuration the australopithecines are all closer to one another than are any of them to arboreal forms such as the orang-utan. It is presumably far more likely that the patterns of uniqueness and diversity that have been uncovered relate to biomechanical aspects of behavior.
The results speak, therefore, to the following deductions. These australopithecines, in displaying uniqueness in morphology, may likewise have been functionally unique from all living hominoids. This may mean that they were not arboreal in the different manners of the Asiatic apes; it surely means they were not terrestrial in the special knuckle-walking mode of the African apes; they cannot have been solely bipedal like a man. They, therefore, displayed either a totally new and unknown manner of locomotion which would be unique in its own right (and which we will judge unlikely), or they possessed such a mixture of locomotor abilities, therefore anatomical adaptations, and therefore, in turn, bony morphologies, as to be rendered unique through being curious functional and morphological mosaics.
The modes in which they are similar to man indicate propensities for a type of bipedality. But the differences indicate that this bipedal activity was not similar to that of man. The ways in which they are similar to the arboreal apes indicate abilities for quadrupedal movement, presumably in an arboreal environment and with a degree of acrobatic climbing. But, again, the differences indicate that this was not in the same manner as any present-day arboreal ape.
Let us be clear that these suggestions do not include merely an extension of human capabilities. Humans can climb using methods like those of apes rather than most monkeys, but our abilities to live in a climbing setting are almost non-existent. Likewise, we can, and do, when infants, move on all four limbs; but, in fact, our quadrupedal facility is virtually zero. Our true abilities in both these directions cannot be said by anyone to be other than a total liability in any conceivable, life framework where they would be required. Such was presumably not the case with these australopithecines, although we are not able, from these data, to disentangle the time relationships of the developments.
Conclusion
Various studies re-emphasize the question of the morphological assessment of the genus Tarsius. Is there other major evidence of a close relationship between tarsiers on the one hand and the monkeys, apes, and man on the other, in the structural and functional affinities of these forms? Is evidence of a relationship of Tarsius to the other prosimians absent?
Locomotor convergences in the limbs. A major problem in understanding the meaning of the anatomy of Tarsius is that it is so closely associated with the remarkable form of locomotion that the animal exhibits. So divergent is this locomotor pattern from that of any of the Anthropoidea that structures that may speak to an association of tarsiers with anthropoids may be overshadowed by functional adaptations to this form of leaping. Further, the extreme locomotor pattern of Tarsius seems very closely analogous to that of the bushbaby, undeniably a prosimian. The degree of morphological convergence of Tarsius with such prosimians may hide morphological relationships speaking to its phylogenetic position.
An attempt is therefore made here to study the relationships of these creatures using the very large battery of data about the overall form and proportions of the body. The extent to which it is possible to ‘dissect away’ (to use an anatomical allusion) or to ‘partition out’ (to use a statistical metaphor) morphological convergence associated with an extreme locomotor pattern may provide another view of the affinities of the genus.
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