Protocol to record and analyze primate leaping in three-dimensional in the wild.

Several studies comparing primate locomotion under lab versus field conditions have shown the importance of implementing both types of studies, as each has their advantages and disadvantages. However, three-dimensional (3D) motion capture of primates has been challenging under natural conditions. In this study, we provide a detailed protocol on how to collect 3D biomechanical data on primate leaping in their natural habitat that can be widely implemented. To record primate locomotion in the dense forest we use modified GoPro Hero Black cameras with zoom lenses that can easily be carried around and set up on tripods. We outline details on how to obtain camera calibrations at greater heights and how to process the collected data using the MATLAB camera calibration app and the motion tracking software DLTdv8a. We further developed a new MATLAB application "WildLeap3D" to generate biomechanical performance metrics from the derived x, y, z coordinates of the leaps. We provide details on how to collect data on support diameter, compliance, and orientation, and combine these with the jumps to study locomotor performance in an ecological context. We successfully reconstructed leaps of wild primates in the 3D space under natural conditions and provided data on four representative leaps. We provide exemplar data on primate velocity and acceleration during a leap and show how our protocol can be used to analyze segmental kinematics. This study will help to make motion capture of freely moving animals more accessible and help further our knowledge about animal locomotion and movement.

Pump and sway: Wild primates use compliant supports as a tool to augment leaping in the canopy.

OBJECTIVES: Despite qualitative observations of wild primates pumping branches before leaping across gaps in the canopy, most studies have suggested that support compliance increases the energetic cost of arboreal leaping, thus limiting leaping performance. In this study, we quantified branch pumping behavior and tree swaying in wild primates to test the hypothesis that these behaviors improve leaping performance. MATERIALS AND METHODS: We recorded wild colobine monkeys crossing gaps in the canopy and quantitatively tracked the kinematics of both the monkey and the compliant support during behavioral sequences. We also empirically measured the compliance of a sample of locomotor supports in the monkeys' natural habitat, allowing us to quantify the resonant properties of substrates used during leaping. RESULTS: Analyses of three recordings show that adult red colobus monkeys (Piliocolobus tephrosceles) use branch compliance to their advantage by actively pumping branches before leaping, augmenting their vertical velocity at take-off. Quantitative modeling of branch resonance periods, based on empirical measurements of support compliance, suggests that monkeys specifically employed branch pumping on relatively thin branches with protracted periods of oscillation. Finally, an additional four recordings show that both red colobus and black and white colobus monkeys (Colobus guereza) utilize tree swaying to cross large gaps, augmenting horizontal velocity at take-off. DISCUSSION: This deliberate branch manipulation to produce a mechanical effect for stronger propulsion is consistent with the framework of instrumental problem-solving. To our knowledge, this is the first study of wild primates which quantitatively shows how compliant branches can be used advantageously to augment locomotor performance.

From such great heights: The effects of substrate height and the perception of risk on lemur locomotor mechanics.

OBJECTIVES: An accident during arboreal locomotion can lead to risky falls, but it remains unclear that the extent to which primates, as adept arborealists, change their locomotion in response to the perceived risk of moving on high supports in the tree canopy. By using more stable forms of locomotion on higher substrates, primates might avoid potentially fatal consequences. MATERIALS AND METHODS: Using high-speed cameras, we recorded the quadrupedal locomotion of four wild lemur species-Eulemur rubriventer, Eulemur rufifrons, Hapalemur aureus, and Lemur catta (N = 113 total strides). We quantified the height, diameter, and angular orientation of locomotor supports using remote sensors and tested the influence of support parameters on gait kinematics, specifically predicting that in response to increasing substrate height, lemurs would decrease speed and stride frequency, but increase stride length and the mean number of supporting limbs. RESULTS: Lemurs did not adjust stride frequency on substrates of varying height. Adjustments to speed, stride length, and the mean number of supporting limbs in response to varying height often ran counter to predictions. Only E. rubriventer decreased speed and increased the mean number of supporting limbs on higher substrates. DISCUSSION: Results suggest that quadrupedal walking is a relatively safe form of locomotion for lemurs, requiring subtle changes in gait to increase stability on higher-that is, potentially riskier-substrates. Continued investigation of the impact of height on locomotion will be important to determine how animals assess risk in their environment and how they choose to use this information to move more safely.

Evaluating The Precocial-altricial Axis of Motor Skill at Birth in A Preterm Pig Model.

The pace of locomotor development is a critical component of lifetime evolutionary fitness. Developmental researchers often divide species into two broad categories based on functional competence at birth: precocial infants who can independently stand and locomote soon after birth versus altricial infants who are either incapable of independent movement or can only do so in a rudimentary manner. However, investigating the lower level neuromotor and biomechanical traits that account for perinatal variation in motor development is complicated by the lack of experimental control inherent to all comparative analyses. Precocial and altricial animals often differ along a host of dimensions that can obfuscate the specific factors controlling motor development per se. Here, we propose an alternative approach of examining locomotor development in a nominally precocial species-the domestic pig (Sus scrofa)-in which gestation length has been experimentally manipulated, thereby creating "functionally altricial" cohorts for comparison. We have used standard biomechanical testing to evaluate balance and locomotor performance in preterm pigs born at 94% full-term gestation (N = 29 individuals) and compared these data to a similar dataset on age-matched full-term piglets (N = 15 individuals). Static balance tests showed that preterm pigs were characterized by increased postural sway, particularly in the fore-aft (anteroposterior) direction. Locomotor analyses showed that preterm piglets tended to take shorter, more frequent strides, use higher duty factors, and preferentially choose gait patterns that ensured they were supported by at least three limbs during most of the stride cycle, though differences between preterm and full-term animals were often modulated by variation in locomotor speed. Morphometric analysis showed no differences in relative extensor muscle mass between preterm and full-term animals, suggesting that neurological immaturity might be more determinant of preterm piglet motor dysfunctions than musculoskeletal immaturity per se (though much work remains to be done to fully document the neuromotor phenotype of the preterm infant pig model). In many ways, the postural and locomotor deficits shown by the preterm piglets paralleled the locomotor phenotype of altricial mammals. Overall, our study demonstrates the utility of a "within-species" design for studying the biomechanical correlates and neuromotor basis of evolutionary variation in motor skill at birth.

Robust locomotor performance of squirrel monkeys (Saimiri boliviensis) in response to simulated changes in support diameter and compliance.

Arboreal environments require overcoming navigational challenges not typically encountered in other terrestrial habitats. Supports are unevenly distributed and vary in diameter, orientation, and compliance. To better understand the strategies that arboreal animals use to maintain stability in this environment, laboratory researchers must endeavor to mimic those conditions. Here, we evaluate how squirrel monkeys (Saimiri boliviensis) adjust their locomotor mechanics in response to variation in support diameter and compliance. We used high-speed cameras to film two juvenile female monkeys as they walked across poles of varying diameters (5, 2.5, and 1.25 cm). Poles were mounted on either a stiff wooden base ("stable" condition) or foam blocks ("compliant" condition). Six force transducers embedded within the pole trackway recorded substrate reaction forces during locomotion. We predicted that squirrel monkeys would walk more slowly on narrow and compliant supports and adopt more "compliant" gait mechanics, increasing stride lengths, duty factors, and an average number of limbs gripping the support, while the decreasing center of mass height, stride frequencies, and peak forces. We observed few significant adjustments to squirrel monkey locomotor kinematics in response to changes in either support diameter or compliance, and the changes we did observe were often tempered by interactions with locomotor speed. These results differ from a similar study of common marmosets (i.e., Callithrix jacchus, with relatively poor grasping abilities), where variation in diameter and compliance substantially impacted gait kinematics. Squirrel monkeys' strong grasping apparatus, long and mobile tails, and other adaptations for arboreal travel likely facilitate robust locomotor performance despite substrate precarity.