Diagonal Sequence Gaits Research Articles

Gaits of Japanese macaques (Macaca fuscata) on a horizontal ladder and arboreal stability

Most primates use diagonal sequence (DS), diagonal couplets (DC) gaits when they walk or run quadrupedally, and it has been suggested that DSDC gaits contribute to stability in their natural arboreal habitats compared to other symmetrical gaits. However, this postulate is based solely on studies of primate gaits using continuous terrestrial and arboreal substrates. A particular species may select suitable gaits according to the substrate properties. Here, we analyzed the gaits of Japanese macaques moving on a horizontal ladder with rung intervals ranging from 0.40 to 0.80 m to elucidate the relative advantages of each observed form of gait. The rung arrangement forced our macaques to choose either diagonal coupling or DS gaits. One macaque consistently used diagonal coupling (i.e., DSDC and LSDC gaits) across narrow and intermediate rung intervals, whereas the other macaque used DS gaits (i.e., DSDC and DSLC gaits). At wider rung intervals, both macaques shifted to a two-one sequence (TOS), which is characterized by two nearly simultaneous touchdowns of both forelimbs and one touchdown of each hind limb in a stride. The transition to the TOS sequence increased the duration of support on multiple limbs, but always included periods of a whole-body aerial phase. These results suggest that Japanese macaques prefer DSDC gaits, because the diagonal coupling and DS contribute separately to stability on complex supports compared to the lateral coupling and lateral sequence. We also postulate that stability triggers the transition from symmetrical gaits to the TOS sequence.

Symmetrical gaits of Cebus apella: implications for the functional significance of diagonal sequence gait in primates

Quadrupedal locomotion of primates is distinguished from the quadrupedalism of many other mammals by several features, including a diagonal sequence (DS) footfall used in symmetrical gaits. This presumably unique feature of primate locomotion has been attributed to an ancestral adaptation for cautious arboreal quadrupedalism on thin, flexible branches. However, the functional significance of DS gait remains largely hypothetical. The study presented here tests hypotheses about the functional significance of DS gait by analyzing the gait mechanics of a primate that alternates between DS and lateral sequence (LS) gaits, Cebus apella. Kinematic and kinetic data were gathered from two subjects as they moved across both terrestrial and simulated arboreal substrates. These data were used to test four hypotheses: (1) locomotion on arboreal supports is associated with increased use of DS gait, (2) DS gait is associated with lower peak vertical substrate reaction forces than LS gait, (3) DS gait is associated with greater forelimb/hind limb differentiation in force magnitudes, and (4) DS gait offers increased stability. Our results indicate that animals preferred DS gait on the arboreal substrate, and LS gait while on the ground. Peak vertical substrate reaction forces showed a tendency to be lower in DS gait, but not consistently so. Pole (“arboreal”) forces were lower than ground forces in DS gait, but not in LS gait. The preferred symmetrical gait on both substrates was a grounded run or amble, with the body supported by only one limb throughout most of the stride. During periods of bilateral support, the DS gait had predominantly diagonal support couplets. This benefit for stability on an arboreal substrate is potentially outweighed by overstriding, its associated ipsilateral limb interference in DS gait and hind foot positioning in front of the hand on untested territory. DS gait also did not result in an optimal anchoring position of the hind foot under the center of mass of the body at forelimb touchdown. In sum, the results are mixed regarding the superiority of DS gait in an arboreal setting. Consequently, the notion that DS gait is an ancestral adaptation of primates, conditioned by the selection demands of an arboreal environment, remains largely hypothetical.

Gait parameter adjustments of cotton‐top tamarins (Saguinus oedipus, Callitrichidae) to locomotion on inclined arboreal substrates

The influence of different substrate inclinations on gaits and metric gait parameters (relative forelimb and hind limb protraction, relative forelimb, and hind limb retraction, stride length, stance, and swing phase duration) of cotton-top tamarin locomotion was studied using high-speed video films and evaluated by descriptive and analytical statistical methods. As previously shown, lateral sequence gaits predominantly occurred on descending arboreal substrates (branchlike pole with a smaller diameter than the animal's body). Gait sequence patterns display significant dependency on substrate inclination. Cotton-top tamarins utilize lower diagonality values the more the substrate declines. This tendency leads to a greater use of lateral sequence gaits on steeply declined substrates. Conversely, these primates display the tendency to utilize higher diagonality values the more the substrate inclines leading to the predominant occurrence of diagonal sequence (DS) gaits. Duty factor index, extent of relative protraction, and relative retraction of both limb pairs as well as the relation of forelimb stance phase duration to hind limb stance phase duration is also correlated to the inclination of the substrate. Stride length and swing phase duration display no significant dependence on inclination, but are determined by the speed of the moving animal. The relevant duty factor is approximately constant at all inclinations. Integrating our results with results of other authors we propose a hypothesis for the functional relevance of a utilization of lateral sequence gaits in downward locomotion and DS gaits in upward locomotion. Our data support the notion of a wide ranging behavioral plasticity as a general primate locomotor characteristic.

The effect of branch diameter on primate gait sequence pattern

Most mammals use lateral sequence gaits during quadrupedal locomotion, a pattern characterized by the touchdown of a forelimb directly following the ipsilateral hind limb in a given stride cycle. Primates, however, tend to use diagonal sequence (DS) gaits, whereby it is the touchdown of a contralateral forelimb that follows that of a given hind limb most closely in time. A number of scenarios have been offered to explain why primates favor DS gaits, most of them relating to the use of the arboreal habitat and, in particular, the exploitation of a narrow branch niche. This experimental study explores the potential explanation for the use of DS gaits by examining the relationship between branch diameter and gait patterns in 360 strides collected from six species of quadrupedal strepsirrhine primates on broad and narrow diameter supports. Gait sequence is quantified using limb phase, or the percentage of time during a stride cycle that a forelimb touchdown follows an ipsilateral hind limb touchdown. Although Loris, Nycticebus and Eulemur rubriventer individuals in this study did exhibit significantly lower locomotor velocities on narrower supports (P<0.01 in all three species), analyses of covariance showed no significant differences in limb phase values between broad and narrow diameter supports. Hence, results indicate surprisingly little evidence to suggest that alterations in gait sequence pattern provide a specific advantage for negotiating narrow supports.

Body mass distribution and gait mechanics in fat-tailed dwarf lemurs ( Cheirogaleus medius) and patas monkeys ( Erythrocebus patas)

Most quadrupeds walk with lateral sequence (LS) gaits, where hind limb touchdowns are followed by ipsilateral forelimb touchdowns. Primates, however, typically walk with diagonal sequence (DS) gaits, where hind limb touchdowns are followed by contralateral forelimb touchdowns. Because the use of DS gaits is nearly ubiquitous among primates, understanding gait selection in primates is critical to understanding primate locomotor evolution. The Support Polygon Model [Tomita, M., 1967. A study on the movement pattern of four limbs in walking. J. Anthropol. Soc. Nippon 75, 120–146; Rollinson, J., Martin, R.D., 1981. Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symp. Zool. Soc. Lond. 48, 377–427] argues that primates' use of DS gaits stems from a more caudal position of the whole-body center of mass (COM) relative to other mammals. We tested the predictions of the Support Polygon Model by examining the effects of natural and experimental variations in COM position on gait mechanics in two distantly related primates: fat-tailed dwarf lemurs ( Cheirogaleus medius) and patas monkeys ( Erythrocebus patas). Dwarf lemur experiments compared individuals with and without a greatly enlarged tail (a feature associated with torpor that can be expected to shift the COM caudally). During patas monkey experiments, we experimentally shifted the COM cranially with the use of a weighted belt (7–12% of body mass) positioned above the scapulae. Examination of limb kinematics revealed changes consistent with systematic deviations in COM position. Nevertheless, footfall patterns changed in a direction contrary to the predictions of the Support Polygon Model in the dwarf lemurs and did not change at all in the patas monkey. These results suggest that body mass distribution is unlikely to be the sole determinant of footfall pattern in primates and other mammals.

Stability, limb coordination and substrate type: the ecorelevance of gait sequence pattern in primates

The coordination of limb movements during mammalian locomotion has been well documented in the literature. Most mammals use lateral sequence (LS) gaits, in which a forelimb follows an ipsilateral hind limb during the stride cycle. Primates, however, tend to utilize diagonal sequence (DS) gaits, whereby a contralateral forelimb follows a given hind limb during the stride cycle. A number of scenarios have been offered to explain why primates favor DS gaits, most of them relating to the use of the arboreal habitat and, in particular, the exploitation of a terminal branch niche. Yet to date, there is surprisingly little evidence to support the advantage of DS gaits for negotiating different aspects of the terminal branch environment. Nonetheless, it is apparent that primates possess unique morphologies and a higher than typically recognized degree of flexibility in gait sequence pattern, both of which likely offer advantages for moving upon discontinuous and unstable terminal branches. This paper reviews potential explanations for the use of DS gaits in primates and considers mechanisms by which gait sequence may be altered during different types of arboreal challenges.

Locomotor mechanics of the slender loris ( Loris tardigradus)

The quadrupedal walking gaits of most primates can be distinguished from those of most other mammals by the presence of diagonal-sequence (DS) footfall patterns and higher peak vertical forces on the hindlimbs compared to the forelimbs. The walking gait of the woolly opossum ( Caluromys philander), a highly arboreal marsupial, is also characterized by diagonal-sequence footfalls and relatively low peak forelimb forces. Among primates, three species— Callithrix, Nycticebus, and Loris—have been reported to frequently use lateral-sequence (LS) gaits and experience relatively higher peak vertical forces on the forelimbs. These patterns among primates and other mammals suggest a strong association between footfall patterns and force distribution on the limbs. However, current data for lorises are limited and the frequency of DS vs. LS walking gaits in Loris is still ambiguous. To test the hypothesis that patterns of footfalls and force distribution on the limbs are functionally linked, kinematic and kinetic data were collected simultaneously for three adult slender lorises ( Loris tardigradus) walking on a 1.25 cm horizontal pole. All subjects in this study consistently used diagonal-sequence walking gaits and always had higher peak vertical forces on their forelimbs relative to their hindlimbs. These results call into question the hypothesis that a functional link exists between the presence of diagonal-sequence walking gaits and relatively higher peak vertical forces on the hindlimbs. In addition, this study tested models that explain patterns of force distribution based on limb protraction angle or limb compliance. None of the Loris subjects examined showed kinematic patterns that would support current models proposing that weight distribution can be adjusted by actively shifting weight posteriorly or by changing limb stiffness. These data reveal the complexity of adaptations to arboreal locomotion in primates and indicate that diagonal-sequence walking gaits and relatively low forelimb forces could have evolved independently.

WALK ON FOUR LEGS NOT ON TWO

![Figure][1] When walking, most mammalian quadrupeds use lateral-sequence gaits, where hindlimb footfall is followed by the ipsilateral (same-side) forelimb. By contrast, primates generally use what is known as a diagonal-sequence gait; after one hindlimb makes ground contact, the

Footfall patterns and interlimb co‐ordination in opossums (Family Didelphidae): evidence for the evolution of diagonal‐sequence walking gaits in primates

Most primates typically use a diagonal‐sequence footfall pattern during walking. This footfall pattern, which is unusual for mammals, is believed to have originated in ancestral primates in association with the use of grasping extremities for movement and foraging on thin, flexible branches. This theory was tested by comparing gait parameters between the grey short‐tailed opossum Monodelphis domestica and the woolly opossum Caluromys philander, two didelphid marsupials that are strongly differentiated in grasping morphology of the extremities and in their reliance on foraging strategies involving thin branches. One hundred and thirty gait cycles were analysed quantitatively from videotapes of subjects moving quadrupedally on a runway and on poles of different diameters (7 and 28 mm). Duty factor (i.e. duration of the stance phase as a percentage of the stride period) for the forelimb and hindlimb, as well as diagonality (i.e. phase relationship between the forelimb and hindlimb cycles), were calculated for each of these symmetrical gait cycles. We found that the highly terrestrial Monodelphis, like most other non‐primate mammals, relies primarily on lateral‐sequence walking gaits on both runway and poles, and has relatively higher forelimb duty factors. Like primates, the highly arboreal Caluromys uses primarily diagonal‐sequence walking gaits on the runway and pole, with relatively higher hindlimb duty factors and diagonality. The fact that the woolly opossum, a marsupial with primate‐like feet that moves and forages mainly on thin branches, uses primarily diagonal‐sequence gaits when walking supports the view that primate gaits evolved to meet the demands of locomotion on narrow supports. This also demonstrates the functional role of a grasping foot, in association with relatively higher hindlimb duty factors, protraction, and substrate reaction forces, in the production of such walking gaits.

Origins of primate locomotion: gait mechanics of the woolly opossum.

The locomotion of primates differs from that of other mammals in three fundamental ways. During quadrupedal walking, primates use diagonal sequence gaits, protract their arms more at forelimb touchdown, and experience lower vertical substrate reaction forces on their forelimbs relative to their hindlimbs. It is widely held that the unusual walking gaits of primates represent a basal adaptation for movement on thin, flexible branches and reflect a major change in the functional role of the forelimb. However, little data on nonprimate arboreal mammals exist to test this notion. To that end, we examined the gait mechanics of the woolly opossum (Caluromys philander), a marsupial convergent with small-bodied prosimians in ecology, behavior, and morphology. Data on the footfall sequence, relative arm protraction, and peak vertical substrate reaction forces were obtained from videotapes and force records for three adult woolly opossums walking quadrupedally on a wooden runway and a thin pole. For all steps recorded on both substrates, woolly opossums always used diagonal sequence walking gaits, protracted their arms beyond 90 degrees relative to horizontal body axis, and experienced peak vertical substrate reaction forces on forelimbs that were significantly lower than on hindlimbs. The woolly opossum is the first nonprimate mammal to show locomotor mechanics that are identical to those of primates. This case of convergence between primates and a committed fine-branch, arboreal marsupial strongly implies that the earliest primates evolved gait specializations for fine-branch locomotion, which reflect important changes in forelimb function.

Lateral bending of the lumbar spine during quadrupedalism in strepsirhines

Much research has been devoted to spinal kinematics of nonmammalian vertebrates, while comparatively little is known about the locomotor role of spinal movements in mammals, especially primates. This study, conducted at the Duke University Primate Center, examines the function of lateral spinal bending during quadrupedal walking among a diverse sample of strepsirhines. The taxa studied include Loris tardigradus (1), Nycticebus coucang (1), N. pygmaeus (1),Cheirogaleus medius (2), Varecia variegata (2), Eulemur fulvus (2), and a total sample size of 261 strides. Lateral bending varies among the taxa with respect to both magnitude and effects of velocity, and does not appear to be correlated with body size. In addition, the timing of lateral bending during a stride appears to differ from that reported for other (nonmammalian) tetrapods. On average, maximum lateral flexion occurs just after ipsilateral foot touchdown, which may be functionally associated with touchdown of the contralateral forelimb during diagonal sequence gait. For some of the taxa, lateral flexion coincides more closely with foot touchdown as velocity increases, suggesting a functional role in increasing hindlimb stride length. Both of these timing patterns contrast with those reported for lizards. Finally, although lorids as a group have been described as having a “sinuous” gait, this study shows more pronounced lateral flexion in Nycticebus than in Loris.

Squirrel monkey locomotion on an inclined treadmill: Implications for the evolution of gaits

Abstract Three adult squirrel monkeys were trained to run on a motor-driven treadmill that was inclined downwardly and upwardly at 8°, 16° and 28°, and horizontally (0°). Films were used to compare the gait and kinematics of the animals across the inclines. All three animals used both lateral and diagonal sequence gaits, although the former was preferred at all but the upward 16° and 28° inclines. Cycle duration and hind limb stance and swing durations tended to increase as downward inclination decreased. Trunk inclination, except at 28° downward, tended to parallel the changes in treadmill inclination. The most dramatic and consistent change for the hind limb joint displacement patterns was that maximum extension during stance increased as the treadmill inclination increased from 28° downward to 28° upward. In contrast to an earlier study by Prost & Sussman (1969), we could find no evidence that squirrel monkeys are best adapted to run on upward inclines of about 16°. The utilization of diagonal sequence gaits on the upward inclines supports previous suggestions that the preference for these gaits in primates is associated with an evolutionary increase in climbing behaviors.

A critique of the walk pattern analysis of symmetrical quadrupedal gaits

The walk pattern method of symmetrical gait analysis does not differentiate between lateral sequence and diagonal sequence gaits in which the forefoot support patterns are identical. Therefore, it is necessary to indicate the sequence of support posture. Gaits of similar support sequence but with different proportions of fore- to hindfoot support per stride are likely to be statistically different. Additional support postures can be incorporated in the walk pattern, thereby permitting a comparison of running and asymmetrical gaits.