How the cubic measure of the jumping style of the prosimian and its proportions is determined

How does body size determine the locomotor performance and proportions of leapers? In an analysis of the mechanics of leaping we derived two principles that explain the kinematic and morphological differences between leaping prosimian primates of different body size. 1. In small animals, the distance through which the body can be accelerated during take-off, and the time available for acceleration, are short. In small-bodied leapers we therefore find adaptations that increase the distance or length of time for propulsion and maximize speed. These are: great angular excursions at the joints of the hindlimb, long load arms of body weight and short power arms for the muscles, elongated hindlimbs with a disproportionate lengthening of the distal segments, and additional joints in the tarsus. 2. With increasing body size, the time for accelerating the body is no longer a problem. Instead, the ratio of muscle force available for acceleration to mass to be accelerated is unfavorable. Accordingly, large-bodied leapers have adaptations that allow optimal use of available muscle force. These include: acceleration in energetically profitable joint positions, avoidance of acute joint angles especially at the distal joints (where the muscles work against the highest percentage of body mass), only moderate elongation of the hindlimbs with rather short distal segments, and long lever arms of those muscles that extend the hindlimb joints. In addition, take-offs of the larger-bodied leapers are characterized by a regularly occurring arm swing movement, thus making additional use of nonhindlimb muscles for acceleration. The mass-dependent differences in forces and velocities have consequences for the energy budget. As the muscles of the small species must contract very rapidly against high loads, they consume more energy per unit of mechanical work. It is not possible to optimize speed and force in the same animal. Body size in conjunction with the laws of mechanics determines how maximum leaping potential will be realized.     

Takeoff and landing forces of leaping strepsirhine primates.

Knowledge of the forces animals generate and are exposed to during locomotion is an important prerequisite for understanding the musculoskeletal correlates of locomotor modes. We recorded takeoff and landing forces for 14 animals representing seven species of strepsirhine primates with a compliant force pole. Our sample included both specialized vertical clingers and leapers and more generalized species. Takeoff forces are higher than landing forces. Peak forces during acceleration for takeoff ranged from 6 to 12 times body weight, and the peak impact forces at landing are between 5 and 9 times body weight. There is a size-related trend in peak force magnitudes. Both takeoff and landing forces decrease with increasing body size in our sample of animals from 1 kg to over 5 kg. Peak forces increase with distance leapt. The distance effect is less clear, probably due to the narrow range of distances represented in our sample. A comparison of subadult and adult animals of two species of sifakas reveals a tendency for the young animals to exert relatively higher peak forces in comparison to their adult conspecifics. Finally, Lemur catta and Eulemur rubriventer, the "generalists" in our sample, tend to generate higher forces for equal tasks than the specialized vertical clingers and leapers (i.e., the indriids and Hapalemur).A broad-scale comparison of peak leaping forces and peak forces for quadrupedal and bipedal walking and running shows that leaping at small body size is associated with exceptionally high forces. Whereas relative forces (i.e., forces divided by body weight) decrease with increasing body mass for leaping, forces for walking and running do not change much with size. Leaping forces in our sample scale to (mass)(-1/3), which is consistent with expectations derived from geometric similarity models. Forces associated with other locomotor activities do not appear to follow this pattern. The very high forces found in strepsirhine leapers do not seem to be matched by bone robusticity beyond that documented for quadrupedal species.     

Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.     

Center of mass motion in swimming fish: effects of speed and locomotor mode during undulatory propulsion

Studies of center of mass (COM) motion are fundamental to understanding the dynamics of animal movement, and have been carried out extensively for terrestrial and aerial locomotion. But despite a large amount of literature describing different body movement patterns in fishes, analyses of how the center of mass moves during undulatory propulsion are not available. These data would be valuable for understanding the dynamics of different body movement patterns and the effect of differing body shapes on locomotor force production. In the present study, we analyzed the magnitude and frequency components of COM motion in three dimensions (x: surge, y: sway, z: heave) in three fish species (eel, bluegill sunfish, and clown knifefish) swimming with four locomotor modes at three speeds using high-speed video, and used an image cross-correlation technique to estimate COM motion, thus enabling untethered and unrestrained locomotion. Anguilliform swimming by eels shows reduced COM surge oscillation magnitude relative to carangiform swimming, but not compared to knifefish using a gymnotiform locomotor style. Labriform swimming (bluegill at 0.5 body lengths/s) displays reduced COM sway oscillation relative to swimming in a carangiform style at higher speeds. Oscillation frequency of the COM in the surge direction occurs at twice the tail beat frequency for carangiform and anguilliform swimming, but at the same frequency as the tail beat for gymnotiform locomotion in clown knifefish. Scaling analysis of COM heave oscillation for terrestrial locomotion suggests that COM heave motion scales with positive allometry, and that fish have relatively low COM oscillations for their body size.     

Comparative locomotion of six sympatric primates in Ecuador

Primates exhibit a great variety of arboreal locomotor modes associated with their size and postcranial morphology. The study of sympatric primates is interesting in that it may reveal how primates of different sizes and anatomies move and select for forest structure. This study reports on preliminary data on the locomotion of six non-ateline platyrrhines found in the Yasuni National Park, Napo Province, Ecuador. Pygmy marmosets are confined to the understory using scansorial locomotion and quadrupedalism, preferring large vertical supports. Golden-mantled tamarins, common squirrel monkeys and dusky titis also range in the understory, moving by quadrupedal walk and leap, mainly on small horizontal supports. Monk sakis are found in the main canopy and use quadrupedal walk and less leap on medium-sized horizontal supports. Whitefronted capuchins use the understory and the main canopy equally often, walking quadrupedally and leaping on small and medium-sized oblique supports. In general, smaller species occupy lower strata while larger species tend to spend more time in the upper strata. Small tegulae-bearing monkeys showed the highest proportions of large vertical support use. For all species, leaping was the main gap-crossing mode, though decreasing in proportion with a higher use of the upper forest layers.     

Body shape and differences between species

The variation of body shape among prosimians is reviewed. Special emphasis is placed on the selective advantages, that is the mechanical reasons, to which variants of the locomotor apparatus can be traced back. There are differences found in the cheiridia, but at present they cannot be explained in terms of mechanics; there is nearly no knowledge about the mechanical meaning of their diversity. Myological characteristics of taxa can be explained mechanically, but this has not yet been done. Well known are variations of body proportions. These discriminate higher taxa, and are largely coincident with the often-used locomotor categories. In spite of this, there are only few sound arguments about the real biomechanic value of characteristic proportions for a given locomotor mode. What is known on this field, is reviewed. Progress can be made only, if the mechanical conditions, set by postural behavior and locomotion, are understood completely. The subtle distinctions between lower taxonomic units can normally be identified only on the basis of detailed and quantified analyses of movements on one hand, and of biometrics on the other. In the few cases in which such studies have been made, the differences of morphology fit to the mechanical requirements of locomotion which also differ only in quantitative details.     

Influences of limb proportions and body size on locomotor kinematics in terrestrial primates and fossil hominins

During locomotion, mammalian limb postures are influenced by many factors including the animal's limb length and body mass. Polk (2002) compared the gait of similar-sized cercopithecine monkeys that differed limb proportions and found that longer-limbed monkeys usually adopt more extended joint postures than shorter-limbed monkeys in order to moderate their joint moments. Studies of primates as well as non-primate mammals that vary in body mass have demonstrated that larger animals use more extended limb postures than smaller animals. Such extended postures in larger animals increase the extensor muscle mechanical advantage and allow postures to be maintained with relatively less muscular effort (Polk, 2002; Biewener 1989). The results of these previous studies are used here to address two anthropological questions. The first concerns the postural effects of body mass and limb proportion differences between australopithecines and members of the genus Homo. That is, H. erectus and later hominins all have larger body mass and longer legs than australopithecines, and these anatomical differences suggest that Homo probably used more extended postures and probably required relatively less muscular force to resist gravity than the smaller and shorter-limbed australopithecines. The second question investigates how animals with similar size but different limb proportions differ in locomotor performance. The effects of limb proportions on gait are relevant to inferring postural and locomotor differences between Neanderthals and modern Homo sapiens which differ in their crural indices and relative limb length. This study demonstrates that primates with relatively long limbs achieve higher walking speeds while using lower stride frequencies and lower angular excursions than shorter-limbed monkeys, and these kinematic differences may allow longer-limbed taxa to locomote more efficiently than shorter-limbed species of similar mass. Such differences may also have characterized the gait of Homo sapiens in comparison to Neanderthals, but more experimental data on humans that vary in limb proportions are necessary in order to evaluate this question more thoroughly.     

Positional behavior of free-ranging Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Positional behavior was quantitatively studied in identified free-ranging Japanese macaques (Macaca fuscata). Five male and 11 female adults were observed in a forested mountain habitat. Data were analyzed for proportion of bout distance, number and time of each locomotion and postural type. Japanese macaques are semiterrestrial, and mainly walk and run quadrupedally. This supports the notion that Macaca are generally quadrupeds. Sex differences in positional behavior were found in the preference of substrate and types of positional behavior. Males and females tend to be terrestrial and arboreal, respectively. Males leap more frequently and longer in distance than do females when they are feeding in trees. These sex differences are considered to be related to differences in morphology, food choice, social activity, and the nursing of infants. Frequencies of leaping and the distance covered by leaping in Japanese macaques are more than those of long-tailed macaques which are arboreal quadrupeds. However, Japanese macaques leap shorter distances at a time than do long-tailed macaques, which indicates that body size may be related to leaping distance more than the frequency of leaping and the distance covered by leaping. Japanese macaques are not as specialized for terrestrial locomotion as pig-tailed macaques. They use both terrestrial and arboreal supports, and are considered to be semi-terrestrial quadrupeds, somewhere between the arboreal long-tailed macaque and the terrestrial pig-tailed macaque. Electronic Publication     

Functional aspects of strepsirrhine lumbar vertebral bodies and spinous processes

The relationship between form and function in the lumbar vertebral column has been well documented among platyrrhines and especially catarrhines, while functional studies of postcranial morphology among strepsirrhines have concentrated predominantly on the limbs. This morphometric study investigates biomechanically relevant attributes of the lumbar vertebral morphology of 20 species of extant strepsirrhines. With this extensive sample, our goal is to address the influence of positional behavior on lumbar vertebral form while also assessing the effects of body size and phylogenetic history. The results reveal distinctions in lumbar vertebral morphology among strepsirrhines in functional association with their habitual postures and primary locomotor behaviors. In general, strepsirrhines that emphasize pronograde posture and quadrupedal locomotion combined with leaping (from a pronograde position) have the relatively longest lumbar regions and lumbar vertebral bodies, features promoting sagittal spinal flexibility. Indrids and galagonids that rely primarily on vertical clinging and leaping with orthograde posture share a relatively short (i.e., stable and resistant to bending) lumbar region, although the length of individual lumbar vertebral bodies varies phylogenetically and possibly allometrically. The other two vertical clingers and leapers, Hapalemur and Lepilemur, more closely resemble the pronograde, quadrupedal taxa. The specialized, suspensory lorids have relatively short lumbar regions as well, but the lengths of their lumbar regions are influenced by body size, and Arctocebus has dramatically longer vertebral bodies than do the other lorids. Lumbar morphology among galagonids appears to reflect a strong phylogenetic signal superimposed on a functional one. In general, relative length of the spinous processes follows a positively allometric trend, although lorids (especially the larger-bodied forms) have relatively short spinous processes for their body size, in accordance with their positional repertoire. The results of the study broaden our understanding of postcranial adaptation in primates, while providing an extensive comparative database for interpreting vertebral morphology in fossil primates.     

Hindlimb proportions, allometry, and biomechanics in Old World monkeys (primates, Cercopithecidae).

The traditional focus on morphological rather than mechanical units has obscured some significant functional differences in the hindlimbs of primates. This paper examines the allometric and biomechanical basis for some distinctive proportional differences among pairs of morphological units in the hindlimb, and especially the foot, of cercopithecid primates. Five major conclusions are reached. First, many hindlimb dimensions scale allometrically with body mass to maintain mechanical similarity within taxonomic and locomotor groups. Therefore, the majority of traditional indices which describe the shape of the foot within cercopithecids reveal differences which are primarily a function of size. Second, the hindlimb segments in colobines, and especially in Presbytis, are relatively long, probably to enhance leaping. Third, the major distinction of terrestrial cercopithecines among the features analysed is reduction in the length of the phalanges, due to the reduced importance of grasping during locomotion and the assumption of digitigrady. Fourth, Theropithecus and male Erythrocebus have high crural indices, relative to their body masses, which can facilitate curosoriality. Female E. patas already has a high crural index as a function of its body mass. Fifth, macaques form a distinctive group among cercopithecines, characterized by relatively short hindlimbs. Relatively very short hindlimbs in Macaca fuscata and M. thibetana suggest that climatic conditions can have an added effect on the lengths of the hindlimb segments. In summary, this analysis of the lengths of the hindlimb segments relative to body size reveals taxonomic differences which are due in part to phylogeny, to differences in locomotor behavior, and to substrate use.     

Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods

A reanalysis of locomotor data from functional, energetic, mechanical and ecological perspectives reveals that limb posture has major effects on limb biomechanics, energy-saving mechanisms and the costs of locomotion. Regressions of data coded by posture (crouched vs. erect) reveal nonlinear patterns in metabolic cost, limb muscle mass, effective mechanical advantage, and stride characteristics. In small crouched animals energy savings from spring and pendular mechanisms are inconsequential and thus the metabolic cost of locomotion is driven by muscle activation costs. Stride frequency appears to be the principal functional parameter related to the decreasing cost of locomotion in crouched animals. By contrast, the shift to erect limb postures invoked a series of correlated effects on the metabolic cost of locomotion: effective mechanical advantage increases, relative muscle masses decrease, metapodial limb segments elongate dramatically (as limbs shift from digitigrade to unguligrade designs) and biological springs increase in size and effectiveness. Each of these factors leads to decreases in the metabolic cost of locomotion in erect forms resulting from real and increasing contributions of pendular savings and spring savings. Comparisons of the relative costs and ecological relevance of different gaits reveal that running is cheaper than walking in smaller animals up to the size of dogs but running is more expensive than walking in horses. Animals do not necessarily use their cheapest gaits for their predominant locomotor activity. Therefore, locomotor costs are driven more by ecological relevance than by the need to optimize locomotor economy.     

Explosive jumping: extreme morphological and physiological specializations of Australian rocket frogs (Litoria nasuta)

Abstract Anuran jumping is an ideal system for examining the relationships between key morphological, physiological, and kinematic parameters. We used the Australian rocket frog (Litoria nasuta) as a model species to investigate extreme specialization of the vertebrate locomotor system for jumping. We measured the ground reaction forces applied during maximal jumps using a custom-designed force platform, which allowed us to calculate instantaneous measures of acceleration, velocity, power output, and total jump distance. We quantified the mechanical properties of the plantaris longus muscle using the work loop technique. We found that L. nasuta achieved the second-longest relative jumping distance for any anuran (55.2 body lengths for one individual) and the highest published anuran values for isolated net mean muscle power output measured using work loops (93.5 W kg(-1) muscle mass), hindlimb length to snout-vent length ratio (2.02), and relative hindlimb muscle mass (33% of body mass). Litoria nasuta also had a higher ratio of tibia length to snout-vent length than 19 related species. We found that the mean power output expended during the takeoff phase of jumping in the individual that jumped the farthest was about three times greater than our estimate of available muscle power output.     

Evolutionary aspects of primate locomotion

Both neontological and phylogenetic studies are necessary to interpret primate locomotion. Reference to palaeoprimatology and palaeocology, for instance, will lead to a fuller understanding of the roots of such gaits as the vertical clinging and leaping of Tarsius, Indri and Propithecus. Evolutionary trends in posture and locomotion are discussed. The postural trend has been towards maintenance of trunk verticality and the locomotor trend towards an increasing dependence on the forelimbs among arboreal primates. Three stages are recognized in the phylogenetic course of arboreal locomotor adaptation: Stage A. Vertical clinging and leaping; Stage B. Quadrupedalism; Stage C. Brachiation. The role of prehensility of the hand in the evolution of locomotor types is discussed in relation to forest morphology and, in particular, to stratification. Finally a scheme of evolution, set in the framework of ecology, for Old World Monkey groups is presented.     

Leaping behavior of Pithecia pithecia and Chiropotes satanas in eastern Venezuela

I observed leaping behavior in the white-faced saki (Pithecia pithecia) and the black-bearded saki (Chiropotes satanas satanas) for 15 and 10 months, respectively, as part of a larger study of positional behavior in the tribe Pitheciini. I used focal animal instantaneous sampling to observe the two species on separate islands in their natural habitat at Guri Lake, Venezuela. Leaping behavior correlates with patterns of forest use and body size, and differences between the species relate more to habitat preferences than to habitat differences per se. Pithecia usually chose vertical or highly angled supports of lower tree portions for take-off and landing, and took off from a stationary posture. Chiropotes took off from the main crown or terminal branches, gaining momentum from locomotor movement before performing a leaping take-off. Pithecia's vertical body orientation and longer leap distance allowed it to assume a mid-flight tuck to prepare for a hindlimb-first landing onto a solid support, and to absorb landing forces with its relatively longer hindlimbs. Chiropotes remained more pronograde throughout its leaps, and minimized landing forces by landing on all four limbs onto numerous flexible supports in the terminal branches. The smaller-bodied P. pithecia is specialized for vertical clinging and leaping, and exhibits behavioral and morphological parallels with other vertical clingers and leapers. The larger C. satanas is a generalized leaper that lacks morphological specializations for leaping. Pithecia's use of solid supports in the lower tree portions allows it to move quietly through the forest-one of a suite of behaviors related to predator avoidance. This example of variation within one behavioral category has implications for devising locomotor classifications and interpreting fossil remains.     

Scale Effects between Body Size and Limb Design in Quadrupedal Mammals

Recently the metabolic cost of swinging the limbs has been found to be much greater than previously thought, raising the possibility that limb rotational inertia influences the energetics of locomotion. Larger mammals have a lower mass-specific cost of transport than smaller mammals. The scaling of the mass-specific cost of transport is partly explained by decreasing stride frequency with increasing body size; however, it is unknown if limb rotational inertia also influences the mass-specific cost of transport. Limb length and inertial properties – limb mass, center of mass (COM) position, moment of inertia, radius of gyration, and natural frequency – were measured in 44 species of terrestrial mammals, spanning eight taxonomic orders. Limb length increases disproportionately with body mass via positive allometry (length ∝ body mass^0.40); the positive allometry of limb length may help explain the scaling of the metabolic cost of transport. When scaled against body mass, forelimb inertial properties, apart from mass, scale with positive allometry. Fore- and hindlimb mass scale according to geometric similarity (limb mass ∝ body mass^1.0), as do the remaining hindlimb inertial properties. The positive allometry of limb length is largely the result of absolute differences in limb inertial properties between mammalian subgroups. Though likely detrimental to locomotor costs in large mammals, scale effects in limb inertial properties appear to be concomitant with scale effects in sensorimotor control and locomotor ability in terrestrial mammals. Across mammals, the forelimb''s potential for angular acceleration scales according to geometric similarity, whereas the hindlimb''s potential for angular acceleration scales with positive allometry.     

Locomotion and posture in Lagothrix lagotricha

This long-term study of woolly monkey (Lagothrix) locomotor and postural behaviour employs methods identical to those used during a previous study of the locomotion and posture of two species of Ateles, allowing a detailed comparison between the two genera, which are strong competitors in extensive parts of the Amazon basin and northern Andes. As in Ateles, Lagothrix locomotion can be divided into five patterns, based on limb usage: quadrupedal walking and running, suspensory locomotion, climbing, bipedalism (very rare in wild woolly monkeys) and leaping. Lagothrix differs from Ateles primarily in its greater reliance on quadrupedal locomotion during both travel and feeding and on its de-emphasis of the use of suspensory locomotion as compared to Ateles, while the use of climbing and leaping is roughly equal in the two genera. Lagothrix exhibits more generalised (primitive) locomotive behaviour in accordance with its morphology, in comparison to the more specialised Ateles. The generic differences reflect differences in habitat use and particularly foraging ecology.     

Locomotion in some small to medium-sized mammals: a geometric morphometric analysis of the penultimate lumbar vertebra,pelvis and hindlimbs

We assessed the influence of a variety of aspects of locomotion and ecology including gait and locomotor types, maximal running speed, home range, and body size on postcranial shape variation in small to medium-sized mammals, employing geometric morphometric analysis and phylogenetic comparative methods. The four views analyzed, i.e., dorsal view of the penultimate lumbar vertebra, lateral view of the pelvis, posterior view of the proximal femur and proximal view of the tibia, showed clear phylogenetic signal and interesting patterns of association with movement. Variation in home range size was related to some tibia shape changes, while speed was associated with lumbar vertebra, pelvis and tibia shape changes. Femur shape was not related to any locomotor variables. In both locomotor type and high-speed gait analyses, locomotor groups were distinguished in both pelvis and tibia shape analyses. These results suggest that adaptations to both typical and high-speed gaits could explain a considerable portion of the shape of those elements. In addition, lumbar vertebra and tibia showed non-significant relationships with body mass, which suggests that they might be used in morpho-functional analyses and locomotor inferences on fossil taxa, with little or no bias for body size. Lastly, we observed morpho-functional convergences among several mammalian taxa and detected some taxa that achieve similar locomotor features following different morphological paths.     

Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus)

Physiologically related features of muscle morphology are considered with regard to functional adaptation for locomotor and postural behavior in the brown lemur (Lemur fulvus). Reduced physiological cross-sectional area, estimated maximum excursion of the tendon of insertion, length of tendon per muscle fasciculus, and areal fiber type composition were examined in the quadriceps femoris in order to assess the extent of a "division of labor" among four apparent synergists. Each of these four muscles in this prosimian primate displays a distinguishing constellation of morphological features that implies functional specialization during posture and normal locomotion (walk/run, galloping, leaping). Vastus medialis is best suited for rapid whole muscle recruitment and may be reserved for relatively vigorous activities such as galloping and leaping (e.g., small cross-sectional area per mass, long excursion, predominance of fast-low oxidative fibers, relatively little tendon per fasciculus). In theory, rectus femoris could be employed isometrically in order to store elastic strain energy during all phasic activities (e.g., large cross-sectional area per mass, short excursion, predominance of fast-high oxidative fibers, large amount of tendon per fasciculus). Vastus intermedius exhibits an overall morphology indicative of a typical postural muscle (e.g., substantial cross-sectional area, short excursion, predominance of slow-high oxidative fibers, large amount of tendon per fasciculus). The construction of vastus lateralis reflects an adaptation for high force, relatively high velocity, and resistance to fatigue (e.g., large cross-sectional area, long excursion, most heterogeneous distribution of fiber types, large amount of tendon per fasciculus); this muscle is probably the primary contributor to a wide range of locomotor behaviors in lemurs. Marked dramatic architectural disparity among the four bellies, coupled with relative overall fiber type heterogeneity, suggests the potential for exceptional flexibility in muscle recruitment within this mass. One interpretation of this relatively complex neuromuscular organization in the brown lemur is that it represents an adaptation for the exploitation of a three-dimensional arboreal environment by rapid quadrupedalism and leaping among irregular and spatially disordered substrates.