Developmental milestones in captive Galago moholi.

Systems of the body develop in a modular manner. For example, neural development in primates is generally rapid, whereas dental development varies much more. In the present study, we examined development of the skull, teeth, and postcrania in a highly specialized leaping primate, Galago moholi. Eighteen specimens ranging from birth to adult were studied. Bones, teeth, and the cranial cavity (i.e., endocast) were reconstructed with Amira software based on microCT cross-referenced to histology. Amira was also used to compute endocast volume (as a proxy for brain size). Reconstructions of the wrist and ankle show that ossification is complete at 1 month postnatally, consistent with the onset of leaping locomotion in this species. Endocranial volume is less than 50% of adult volume at birth, ~80% by 1 month, and has reached adult volume by 2 months postnatal age. Full deciduous dentition eruption occurs by 2 weeks, and the young are known to begin capturing and consuming arthropods on their own by 4 weeks, contemporaneous with the timing of bone and ankle ossification that accompanies successful hunting. The modular pattern of development of body systems in Galago moholi provides an interesting view of a "race" to adult morphology for some joints that are critical for specialized leaping and clinging, rapid crown mineralization to begin a transitional diet, but perhaps more prolonged reliance on nursing to support brain growth.

Developmental factors influencing bone strength in precocial mammals: An infant pig model.

Most vertebrates are precocial in locomotion, able to walk and run soon after birth. Precociality requires a bony skeleton of sufficient strength to resist mechanical loading during early locomotor efforts. The aim of this study was to use an animal model-the preterm infant pig-to investigate some of the proximate factors that might determine variation in bone strength in precocial animals. Based on the prior literature, we tested the null predictions that skeletal integrity would be significantly compromised by truncated gestation (i.e., preterm birth) and reduced body mass at birth. We generated a suite of both morphometric measures (tissue mineral density and cross-sectional geometry) and performance-related metrics (ability to resist loading, deformation, and fracture during three-point bending tests) of the appendicular skeleton of preterm and full-term infant pigs. Results showed that very few measures in our ontogenetic infant pig sample significantly varied with either gestation length or birth mass. Overall, our results contribute to a growing body of literature demonstrating the early functional capacity of the precocial infant musculoskeletal system and suggest that bone strength in perinatal precocial mammals may be robust to the factors shown to compromise skeletal integrity in more altricial taxa.

Jumping performance in tree squirrels: Insights into primate evolution.

Morphological traits suggesting powerful jumping abilities are characteristic of early crown primate fossils. Because tree squirrels lack certain 'primatelike' grasping features but frequently travel on the narrow terminal branches of trees, they make a viable extant model for an early stage of primate evolution. Here, we explore biomechanical determinants of jumping performance in the arboreal Eastern gray squirrel (Sciurus carolinensis, n = 3) as a greater understanding of the biomechanical strategies that squirrels use to modulate jumping performance could inform theories of selection for increased jumping ability during early primate evolution. We assessed vertical jumping performance by using instrumented force platforms upon which were mounted launching supports of various sizes, allowing us to test the influence of substrate diameter on jumping kinetics and performance. We used standard ergometric methods to quantify jumping parameters (e.g., takeoff velocity, total displacement, peak mechanical power) from force platform data during push-off. We found that tree squirrels display divergent mechanical strategies according to the type of substrate, prioritizing force production on flat ground versus center of mass displacement on narrower poles. As jumping represents a significant part of the locomotor behavior of most primates, we suggest that jumping from small arboreal substrates may have acted as a potential driver of the selection for elongated hindlimb segments in primates, allowing the center of mass to be accelerated over a longer distance-and thereby reducing the need for high substrate reaction forces.

Pump the brakes! The hindlimbs of three-toed sloths decelerate and support suspensory locomotion.

Modern tree sloths are one of few mammalian taxa for which quadrupedal suspension is obligatory. Sloth limb musculature is specialized for slow velocity, large force contractions that stabilize their body below branches and conserve energy during locomotion. However, it is unknown whether two- and three-toed sloths converge in their use of limb kinetics and if these patterns are comparable to how primates perform arboreal suspensory locomotion. This study addressed this need by collecting limb loading data in three-toed sloths (Bradypus variegatus; N=5) during suspensory walking. Sloths performed locomotor trials at their preferred speed on an instrumented beam apparatus with a force platform as the central supporting segment. Peak forces and impulses of the forelimb and hindlimb were recorded and analyzed in three dimensions. The hindlimbs of B. variegatus apply large braking forces greater in magnitude than peak forces generated by the forelimbs in propulsion, a pattern consistent with that observed in two-toed sloths. However, B. variegatus exhibits hindlimb-biased body weight support in vertical peak forces and impulse, with appreciable laterally directed forces in each limb pair, both of which vary from limb loading distributions in two-toed sloths. Moreover, body weight distribution between limb pairs is opposite to that employed by primates during quadrupedal suspension. Thus, there appear to be multiple strategies for achieving suspensory locomotion in arboreal mammals. These differences may be attributable to anatomical variation or phylogenetic position, but as of yet an explanation remains unknown. Future EMG analyses are expected to provide insight into how specific hindlimb muscle groups contribute to braking forces and stabilizing the center of mass of sloths during suspension.

Does a suspensory lifestyle result in increased tensile strength? Organ-level material properties of sloth limb bones.

The material composition of vertebrate connective tissue is highly conserved across taxa. Existing data suggest that the compressive and tensile strength of limb bones are very similar despite marked variation in limb posture and locomotor patterns. However, the material properties of limb bone tissue from suspensory taxa have not been formally evaluated. Sloths are nearly obligatory in their use of below-branch suspensory locomotion and posture, thus placing their limb bones and associated soft tissue structures under routine tensile loading. It is possible that sloth limb bones are modified for enhanced tensile strength, perhaps at the expense of compressive strength. Forelimb and hindlimb bones of two-toed (Choloepus hoffmanni) and three-toed (Bradypus variegatus) sloths were tested in compression and bending to evaluate this hypothesis. Strength and elastic (Young's) modulus were similarly lower in sloth limb bones during both compression and bending, as compared with pronograde taxa. Ratios of peak bending strength to compressive strength additionally were elevated (sloths: 1.4-1.7; upright taxa: 0.6-1.2) for sloth limb bones. Overall, the material properties measured from the limb bones of tree sloths support our hypothesis of predicted function in a tensile limb system. Future studies should aim to directly test bones in tension to confirm indications of elevated axial tensile strength. Nevertheless, the results herein expand understanding of functional adaptation in mammalian tissue for a range of locomotor/postural behaviors that were previously unexplored.

Increased performance in juvenile baboons is consistent with ontogenetic changes in morphology.

OBJECTIVES: In many primates, the greater proportion of climbing and suspensory behaviors in the juvenile repertoire likely necessitates good grasping capacities. Here, we tested whether very young individuals show near-maximal levels of grasping strength, and whether such an early onset of grasping performance could be explained by ontogenetic variability in the morphology of the limbs in baboons. MATERIAL AND METHODS: We quantified a performance trait, hand pull strength, at the juvenile and adult stages in a cross-sectional sample of 15 olive baboons (Papio anubis). We also quantified bone dimensions (i.e., lengths, widths, and heights) of the fore- (n = 25) and hind limb (n = 21) elements based on osteological collections covering the whole development of olive baboons. RESULTS: One-year old individuals demonstrated very high pull strengths (i.e., 200% of the adult performance, relative to body mass), that are consistent with relatively wider phalanges and digit joints in juveniles. The mature proportions and shape of the forelimb elements appeared only at full adulthood (i.e., ≥4.5 years), whereas the mature hind limb proportions and shape were observed much earlier during development. DISCUSSION: These changes in limb performance and morphology across ontogeny may be explained with regard to behavioral transitions that olive baboons experience during their development. Our findings highlight the effect of infant clinging to mother, an often-neglected feature when discussing the origins of grasping in primates. The differences in growth patterns, we found between the forelimb and the hind limb further illustrate their different functional roles, having likely evolved under different ecological pressures (manipulation and locomotion, respectively).

Not all fine-branch locomotion is equal: Grasping morphology determines locomotor performance on narrow supports.

Fine-branch models have long played a central role in primate evolutionary research. Nevertheless, recent studies of positional behavior in nonprimate arboreal mammals have challenged the idea that synapomorphic primate features, such as grasping extremities, uniquely facilitated access to the fine-branch zone. We test the alternative hypothesis that grasping extremities specifically improve locomotor performance in a fine-branch environment by examining how support diameter influences locomotor mechanics in one sciurid rodent (Sciurus carolinensis) and two platyrrhine primates (Callithrix jacchus and Saimiri boliviensis). These species were chosen to broadly model different stages in the evolution of primate grasping morphology. The results showed that transitioning from broad to narrower supports required the greatest kinematic adjustment in squirrels and the least adjustment in squirrel monkeys, with marmosets displaying an intermediate level of adjustment. Moreover, on any given support, squirrels' locomotor mechanics differed from marmosets' in a manner consistent with a greater need for stability, despite superficial ecomorphological similarities between sciurid rodents and callitrichine primates. Morphological analyses of autopodial size and proportions suggest that variation in locomotor performance more closely tracked variation in overall hand and foot size rather than digit length per se. Indeed, a broad comparative analysis revealed that for their body mass, primates have longer hands than similarly sized arboreal rodents and marsupials (although only the primate-rodent comparison was significant after incorporating phylogenetic relatedness). Inclusion of fossil stem primates (plesiadapiforms) and euprimates (adapiforms) in these analyses suggests that this primate-wide grade shift in relative autopodial size must have occurred early in the evolutionary history of the group. Overall, our findings show that basal primate morphological adaptations may have specifically facilitated improved locomotor performance in a fine-branch niche, rather than merely permitting access to the environment. As such, future adaptive hypotheses of primate origins should incorporate the import of primate-like morphology on locomotor performance as well.

Asymmetrical gait kinematics of free-ranging callitrichine primates in response to changes in substrate diameter and orientation.

Arboreal environments present considerable biomechanical challenges for animals moving and foraging among substrates varying in diameter, orientation and compliance. Most studies of quadrupedal gait kinematics in primates and other arboreal mammals have focused on symmetrical walking gaits and the significance of diagonal sequence gaits. Considerably less research has examined asymmetrical gaits, despite their prevalence in small-bodied arboreal taxa. Here, we examined whether and how free-ranging callitrichine primates adjust asymmetrical gait kinematics to changes in substrate diameter and orientation, as well as how variation in gait kinematics affects substrate displacement. We used high-speed video to film free-ranging Saguinus tripartitus and Cebuella pygmaea inhabiting the Tiputini Biodiversity Station, Ecuador. We found that S. tripartitus used bounding and half-bounding gaits on larger substrates versus gallops and symmetrical gaits on smaller substrates, and also shifted several kinematic parameters consistent with attenuating forces transferred from the animal to the substrate. Similarly, C. pygmaea shifted from high-impact bounding gaits on larger substrates to using more half-bounding gaits on smaller substrates; however, kinematic adjustments to substrate diameter were not as profound as in S. tripartitus Both species adjusted gait kinematics to changes in substrate orientation; however, gait kinematics did not significantly affect empirical measures of substrate displacement in either species. Because of their small body size, claw-like nails and reduced grasping capabilities, callitrichines arguably represent extant biomechanical analogs for an early stage in primate evolution. As such, greater attention should be placed on understanding asymmetrical gait dynamics for insight into hypotheses concerning early primate locomotor evolution. .

My branch is your branch: Talar morphology correlates with relative substrate size in platyrrhines at Tiputini Biodiversity Station, Ecuador.

Given that most species of primates are predominantly arboreal, maintaining the ability to move among branches of varying sizes has presumably been a common selective force in primate evolution. However, empirical evaluations of the relationships between morphological variation and characteristics of substrate geometry, such as substrate diameter relative to an animal's body mass, have been limited by the lack of quantified substrate usage in the wild. Here we use recently published quantitative data to assess the relationships between relative substrate size and talar morphology in nine New World monkey species at the Tiputini Biodiversity Station, Ecuador. Within this sample, both fibular facet angle (the angle between the fibular facet and the trochlear rims) and body-mass-standardized area of the medial tibial facet decrease as average and maximum relative substrate size increases. Correlations between medial tibial facet area and relative substrate size are driven by the inclusion of callitrichids in this sample. Nevertheless, these findings strengthen the hypothesis that variation in fibular facet orientation and medial tibial facet area are functionally correlated with habitual degrees of pedal inversion. They also strengthen the notion that evolutionarily changing body mass could impact habitat geometry experienced by a lineage and thereby substantially impact major trends in primate morphological evolution. This study highlights the importance of empirical data on substrate use in living primates for inferring functional and evolutionary implications of morphological variation.

Ontogeny of effective mechanical advantage in eastern cottontail rabbits (Sylvilagus floridanus).

Juvenile animals must survive in the same environment as adults despite smaller sizes, immature musculoskeletal tissues, general ecological naïveté and other limits of performance. Developmental changes in muscle leverage could constitute one mechanism to promote increased performance in juveniles despite ontogenetic limitations. We tested this hypothesis using a holistic dataset on growth and locomotor development in wild eastern cottontail rabbits (Sylvilagus floridanus) to examine ontogenetic changes in hindlimb muscle effective mechanical advantage (EMA). EMA is a dimensionless index of muscle leverage, equal to the quotient of average muscle lever length and the load arm length of the ground reaction force (GRF), effectively representing the magnitude of output force arising from a given muscle force. We found that EMA at the hip and ankle joints, as well as overall hindlimb EMA, significantly declined across ontogeny in S. floridanus, whereas EMA at the knee joint remained unchanged. Ontogenetic decreases in EMA were due to isometric scaling of muscle lever arm lengths alongside positive ontogenetic allometry of GRF load arm lengths - which in turn was primarily related to positive allometry of hindlimb segment lengths. Greater EMA limits the estimated volume of hindlimb extensor muscle that has to be activated in young rabbits, likely mitigating the energetic cost of locomotion and saving metabolic resources for other physiological functions, such as growth and tissue differentiation. An additional examination of limb growth allometry across a diverse sample of mammalian taxa suggests that ontogenetic decreases in limb joint EMA may be a common mammalian trend.

Effects of substrate and phylogeny on quadrupedal gait in free-ranging platyrrhines.

OBJECTIVES: Primate diagonal sequence (DS) gaits are often argued to be an adaptation for moving and foraging in the fine-branch niche; however, existing data have come predominantly from laboratory studies that are limited in taxonomic breadth and fail to account for the structural and ecological variation of natural substrates. We test the extent to which substrate diameter and orientation influence gait sequence type and limb phase in free-ranging primates, as well as how phylogenetic relatedness might condition response patterns. MATERIALS AND METHODS: We filmed quadrupedal locomotion in 11 platyrrhine species at field sites in Ecuador and Costa Rica and measured the diameter and orientation of locomotor substrates using remote sensors. We quantified limb phase values and classified strides by gait sequence type (N = 988 strides). RESULTS: Our results show that most of the species in our sample consistently used DS gaits, regardless of substrate diameter or orientation; however, all taxa also used asymmetrical and/or lateral sequence gaits. By incorporating phylogenetic eigenvectors into our models, we found significant differences in gait sequence patterns and limb phase values among the major platyrrhine clades, suggesting that phylogeny may be a better predictor of gait than substrate diameter or orientation. DISCUSSION: Our field data generally corroborate locomotor patterns from laboratory studies but capture additional aspects of gait variability and flexibility in response to the complexity of natural environments. Overall, our results suggest that DS gaits are not exclusively tailored to narrow or oblique substrates but are used on arboreal substrates in general.

The effects of natural substrate discontinuities on the quadrupedal gait kinematics of free-ranging Saimiri sciureus.

Wild primates encounter complex matrices of substrates that differ in size, orientation, height, and compliance, and often move on multiple, discontinuous substrates within a single bout of locomotion. Our current understanding of primate gait is limited by artificial laboratory settings in which primate quadrupedal gait has primarily been studied. This study analyzes wild Saimiri sciureus (common squirrel monkey) gait on discontinuous substrates to capture the realistic effects of the complex arboreal habitat on walking kinematics. We collected high-speed video footage at Tiputini Biodiversity Station, Ecuador between August and October 2017. Overall, the squirrel monkeys used more asymmetrical walking gaits than symmetrical gaits, and specifically asymmetrical lateral sequence walking gaits when moving across discontinuous substrates. When individuals used symmetrical gaits, they used diagonal sequence gaits more than lateral sequence gaits. In addition, individuals were more likely to change their footfall sequence during strides on discontinuous substrates. Squirrel monkeys increased the time lag between touchdowns both of ipsilaterally paired limbs (pair lag) and of the paired forelimbs (forelimb lag) when walking across discontinuous substrates compared to continuous substrates. Results indicate that gait flexibility and the ability to alter footfall patterns during quadrupedal walking may be critical for primates to safely move in their complex arboreal habitats. Notably, wild squirrel monkey quadrupedalism is diverse and flexible with high proportions of asymmetrical walking. Studying kinematics in the wild is critical for understanding the complexity of primate quadrupedalism.

Use it or lose it? Effects of age, experience, and disuse on crawling.

What happens to early acquired but later abandoned motor skills? To investigate effects of disuse on early-developing motor skills, we examined crawling in two groups of habitual crawlers (34 6-12-month-old infants and five adults with Uner Tan Syndrome) and two groups of rusty crawlers (27 11-12-year-old children and 13 college-aged adults). Habitual crawlers showed striking similarities in gait patterns, limbs supporting the body, and crawling speed, despite dramatic differences in crawling practice, posture, and body size. Habitual crawlers trotted predominantly, whereas rusty crawlers showed a variety of gait patterns. Within sequences, habitual crawlers and children showed more switches in gait patterns than young adults. Children crawled faster and kept fewer limbs on the grounds than the other groups. Old crawling patterns were retained despite disuse, but new ones were also added. Surprisingly, results indicate that nothing was lost with disuse, but some features of crawling were gained or altered.

Developments in development: What have we learned from primate locomotor ontogeny?

The importance of locomotion to evolutionary fitness has led to extensive study of primate locomotor behavior, morphology and ecology. Most previous research has focused on adult primates, but in the last few decades, increased attention to locomotor development has provided new insights toward our broader understanding of primate adaptation and evolution. Here, we review the contributions of this body of work from three basic perspectives. First, we assess possible determinants on the timing of locomotor independence, an important life history event. Significant influences on timing of locomotor independence include adult female body mass, age at weaning, and especially relative brain size, a significant predictor of other primate life history variables. Additionally, we found significant phylogenetic differences in the timing of locomotor independence, even accounting for these influences. Second, we discuss how structural aspects of primate growth may enhance the locomotor performance and safety of young primates, despite their inherent neuromotor and musculoskeletal limitations. For example, compared to adults, growing primates have greater muscle mechanical advantage, greater bone robusticity, and larger extremities with relatively long digits. Third, focusing on primate quadrupedalism, we provide examples that illustrate how ontogenetic transitions in morphology and locomotion can serve as a model system for testing broader principles underlying primate locomotor biomechanics. This approach has led to a better understanding of the key features that contribute to primates' stride characteristics, gait patterns, limb force distribution, and limb postures. We have learned a great deal from the study of locomotor ontogeny, but there is much left to explore. We conclude by offering guidelines for future research, both in the laboratory and the field.

A user's guide for the quantitative analysis of substrate characteristics and locomotor kinematics in free-ranging primates.

OBJECTIVES: Laboratory studies have yielded important insights into primate locomotor mechanics. Nevertheless, laboratory studies fail to capture the range of ecological and structural variation encountered by free-ranging primates. We present techniques for collecting kinematic data on wild primates using consumer grade high-speed cameras and demonstrate novel methods for quantifying metric variation in arboreal substrates. MATERIALS AND METHODS: These methods were developed and applied to our research examining platyrrhine substrate use and locomotion at the Tiputini Biodiversity Station, Ecuador. Modified GoPro cameras equipped with varifocal zoom lenses provided high-resolution footage (1080 p.; 120 fps) suitable for digitizing gait events. We tested two methods for remotely measuring branch diameter: the parallel laser method and the distance meter photogrammetric method. A forestry-grade laser rangefinder was used to quantify substrate angle and a force gauge was used to measure substrate compliance. We also introduce GaitKeeper, a graphical user interface for MATLAB, designed for coding quadrupedal gait. RESULTS: Parallel laser and distance meter methods provided accurate estimations of substrate diameter (percent error: 3.1-4.5%). The laser rangefinder yielded accurate estimations of substrate orientation (mean error = 2.5°). Compliance values varied tremendously among substrates but were largely explained by substrate diameter, substrate length, and distance of measurement point from trunk. On average, larger primates used relatively small substrates and traveled higher in the canopy. DISCUSSION: Ultimately, these methods will help researchers identify more precisely how primate gait kinematics respond to the complexity of arboreal habitats, furthering our understanding of the adaptive context in which primate quadrupedalism evolved.

Extracellular Molecular Markers and Soma Size of Inhibitory Neurons: Evidence for Four Subtypes of GABAergic Cells in the Inferior Colliculus.

Inhibition plays an important role in shaping responses to stimuli throughout the CNS, including in the inferior colliculus (IC), a major hub in both ascending and descending auditory pathways. Subdividing GABAergic cells has furthered the understanding of inhibition in many brain areas, most notably in the cerebral cortex. Here, we seek the same understanding of subcortical inhibitory cell types by combining staining for two types of extracellular markers--perineuronal nets (PNs) and perisomatic rings of terminals expressing vesicular glutamate transporter 2 (VGLUT2)--to subdivide IC GABAergic cells in adult guinea pigs. We found four distinct groups of GABAergic cells in the IC: (1) those with both a PN and a VGLUT2 ring; (2) those with only a PN; (3) those with only a VGLUT2 ring; and (4) those with neither marker. In addition, these four GABAergic subtypes differ in their soma size and distribution among IC subdivisions. Functionally, the presence or absence of VGLUT2 rings indicates differences in inputs, whereas the presence or absence of PNs indicates different potential for plasticity and temporal processing. We conclude that these markers distinguish four GABAergic subtypes that almost certainly serve different roles in the processing of auditory stimuli within the IC. SIGNIFICANCE STATEMENT: GABAergic inhibition plays a critical role throughout the brain. Identification of subclasses of GABAergic cells (up to 15 in the cerebral cortex) has furthered the understanding of GABAergic roles in circuit modulation. Inhibition is also prominent in the inferior colliculus, a subcortical hub in auditory pathways. Here, we use two extracellular markers to identify four distinct groups of GABAergic cells. Perineuronal nets and perisomatic rings of glutamatergic boutons are present in many subcortical areas and often are associated with inhibitory cells, but they have rarely been used to identify inhibitory subtypes. Our results further the understanding of inhibition in the inferior colliculus and suggest that these extracellular molecular markers may provide a key to distinguishing inhibitory subtypes in many subcortical areas.

Effects of support diameter and compliance on common marmoset (Callithrix jacchus) gait kinematics.

Locomotion is precarious in an arboreal habitat, where supports can vary in both diameter and level of compliance. Several previous studies have evaluated the influence of substrate diameter on the locomotor performance of arboreal quadrupeds. The influence of substrate compliance, however, has been mostly unexamined. Here, we used a multifactorial experimental design to investigate how perturbations in both diameter and compliance affect the gait kinematics of marmosets (Callithrix jacchus; N=2) moving over simulated arboreal substrates. We used 3D-calibrated video to quantify marmoset locomotion over a horizontal trackway consisting of variably sized poles (5, 2.5 and 1.25 cm in diameter), analyzing a total of 120 strides. The central portion of the trackway was either immobile or mounted on compliant foam blocks, depending on condition. We found that narrowing diameter and increasing compliance were both associated with relatively longer substrate contact durations, though adjustments to diameter were often inconsistent relative to compliance-related adjustments. Marmosets also responded to narrowing diameter by reducing speed, flattening center of mass (CoM) movements and dampening support displacement on the compliant substrate. For the subset of strides on the compliant support, we found that speed, contact duration and CoM amplitude explained >60% of the variation in substrate displacement over a stride, suggesting a direct performance advantage to these kinematic adjustments. Overall, our results show that compliant substrates can exert a significant influence on gait kinematics. Substrate compliance, and not just support diameter, should be considered a critical environmental variable when evaluating locomotor performance in arboreal quadrupeds.

Grasping primate development: Ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella).

Young primates have relatively large hands and feet for their body size, perhaps enhancing grasping ability. We test the hypothesis that selection for improved grasping ability is responsible for these scaling trends by examining the ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella). If selection for improved grasping ability is responsible for the observed patterns of hand and foot growth in primates, we predicted that fingers and toes would be longer early in life and proportionally decline with age. We measured the lengths of manual and pedal metapodials and phalanges in a mixed-longitudinal radiographic sample. Bone lengths were (a) converted into phalangeal indices (summed non-distal phalangeal length/metapodial length) to test for age-related changes in intrinsic proportions and (b) fit to Gompertz models of growth to test for differences in the dynamics of phalangeal versus metapodial growth. Manual and pedal phalangeal indices nearly universally decreased with age in capuchin monkeys. Growth curve analyses revealed that metapodials generally grew at a faster rate, and for a longer duration, than corresponding phalanges. Our findings are consistent with the hypothesis that primates are under selection for increased grasping ability early in life. Relatively long digits may be functionally adaptive for growing capuchins, permitting a more secure grasp on both caregivers and arboreal supports, as well as facilitating early foraging. Additional studies of primates and other mammals, as well as tests of grasping performance, are required to fully evaluate the adaptive significance of primate hand and foot growth.

Angular momentum and arboreal stability in common marmosets (Callithrix jacchus).

Despite the importance that concepts of arboreal stability have in theories of primate locomotor evolution, we currently lack measures of balance performance during primate locomotion. We provide the first quantitative data on locomotor stability in an arboreal primate, the common marmoset (Callithrix jacchus), predicting that primates should maximize arboreal stability by minimizing side-to-side angular momentum about the support (i.e., Lsup ). If net Lsup becomes excessive, the animal will be unable to arrest its angular movement and will fall. Using a novel, highly integrative experimental procedure we directly measured whole-body Lsup in two adult marmosets moving along narrow (2.5 cm diameter) and broad (5 cm diameter) poles. Marmosets showed a strong preference for asymmetrical gaits (e.g., gallops and bounds) over symmetrical gaits (e.g., walks and runs), with asymmetrical gaits representing >90% of all strides. Movement on the narrow support was associated with an increase in more "grounded" gaits (i.e., lacking an aerial phase) and a more even distribution of torque production between the fore- and hind limbs. These adjustments in gait dynamics significantly reduced net Lsup on the narrow support relative to the broad support. Despite their lack of a well-developed grasping apparatus, marmosets proved adept at producing muscular "grasping" torques about the support, particularly with the hind limbs. We contend that asymmetrical gaits permit small-bodied arboreal mammals, including primates, to expand "effective grasp" by gripping the substrate between left and right limbs of a girdle. This model of arboreal stability may hold important implications for understanding primate locomotor evolution.

Limb bone morphology, bone strength, and cursoriality in lagomorphs.

The primary aim of this study is to broadly evaluate the relationship between cursoriality (i.e. anatomical and physiological specialization for running) and limb bone morphology in lagomorphs. Relative to most previous studies of cursoriality, our focus on a size-restricted, taxonomically narrow group of mammals permits us to evaluate the degree to which 'cursorial specialization' affects locomotor anatomy independently of broader allometric and phylogenetic trends that might obscure such a relationship. We collected linear morphometrics and µCT data on 737 limb bones covering three lagomorph species that differ in degree of cursoriality: pikas (Ochotona princeps, non-cursorial), jackrabbits (Lepus californicus, highly cursorial), and rabbits (Sylvilagus bachmani, level of cursoriality intermediate between pikas and jackrabbits). We evaluated two hypotheses: cursoriality should be associated with (i) lower limb joint mechanical advantage (i.e. high 'displacement advantage', permitting more cursorial species to cycle their limbs more quickly) and (ii) longer, more gracile limb bones, particularly at the distal segments (as a means of decreasing rotational inertia). As predicted, highly cursorial jackrabbits are typically marked by the lowest mechanical advantage and the longest distal segments, non-cursorial pikas display the highest mechanical advantage and the shortest distal segments, and rabbits generally display intermediate values for these variables. Variation in long bone robusticity followed a proximodistal gradient. Whereas proximal limb bone robusticity declined with cursoriality, distal limb bone robusticity generally remained constant across the three species. The association between long, structurally gracile limb bones and decreased maximal bending strength suggests that the more cursorial lagomorphs compromise proximal limb bone integrity to improve locomotor economy. In contrast, the integrity of distal limb bones is maintained with increasing cursoriality, suggesting that the safety factor takes priority over locomotor economy in those regions of the postcranial skeleton that experience higher loading during locomotion. Overall, these findings support the hypothesis that cursoriality is associated with a common suite of morphological adaptations across a range of body sizes and radiations.