Energetic costs of feeding in 12 species of small-bodied primates.

There are no comparative, empirical studies of the energetic costs of feeding in mammals. As a result, we lack physiological data to better understand the selection pressures on the mammalian feeding apparatus and the influence of variables such as food geometric and material properties. This study investigates interspecific scaling of the net energetic costs of feeding in relation to body size, jaw-adductor muscle mass and food properties in a sample of 12 non-human primate species ranging in size from 0.08 to 4.2 kg. Net energetic costs during feeding were measured by indirect calorimetry for a variety of pre-cut and whole raw foods varying in geometric and material properties. Net feeding costs were determined in two ways: by subtracting either the initial metabolic rate prior to feeding or subtracting the postprandial metabolic rate. Interspecific scaling relationships were evaluated using pGLS and OLS regression. Net feeding costs scale negatively relative to both body mass and jaw-adductor mass. Large animals incur relatively lower feeding costs indicating that small and large animals experience and solve mechanical challenges in relation to energetics in different ways. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Point-of-Care Ultrasonography Integration in Undergraduate Medical Education: A Student-Driven Approach.

BACKGROUND: The importance of medical ultrasonography (US) is well established, but given an already dense curriculum, integration of US into preclinical training can be difficult. Although there is no clear consensus on the best practice for integrating US into medical school curricula, growing student interest in US training demands investigation of potential solutions. OBJECTIVE: To investigate whether US integration through peer-assisted learning (PAL) and extracurricular activities during preclinical training is perceived to be valuable by student participants. METHODS: First- and second-year students at the West Virginia School of Osteopathic Medicine (WVSOM) were invited via email to attend 4 monthly PAL extracurricular US sessions on the following point-of-care US topics: (1) basic lung examination to assess pleural sliding, (2) extended focused assessment with sonography for trauma, (3) right upper quadrant biliary examination, and (4) US-guided central venous catheter placement. A brief survey using Likert-style questions inquired about participants' level of agreement with whether the given session was appropriately complex, increased comfort with US, was informative and interactive, and improved confidence in identifying anatomic structures (sessions 2 and 3 only). A final question asked participants whether they would attend more extracurricular US sessions. RESULTS: Fifty-eight students (36 unique students) attended the peer-led sessions. Of the 58 students, 50 responded to the survey for a response rate of 86.2%. Responses were overwhelmingly positive. All respondents strongly agreed or agreed that these sessions improved their confidence in identifying anatomic structures using US, and 49 (98%) strongly agreed or agreed that they would attend more US sessions. CONCLUSION: Respondents strongly endorsed the peer-led US sessions, which has facilitated the formal integration of an elective US course at WVSOM. The peer-led sessions introduced at WVSOM could provide the framework and motivation for similar courses at osteopathic medical schools across the country.

Comparison of spatiotemporal gait characteristics between vertical climbing and horizontal walking in primates.

During quadrupedal walking, most primates utilize diagonal-sequence diagonal-couplet gaits, large limb excursions and hindlimb-biased limb loading. These gait characteristics are thought to be basal to primates, but the selective pressure underlying these gait changes remains unknown. Some researchers have examined these characteristics during vertical climbing and propose that primate quadrupedal gait characteristics may have arisen due to the mechanical challenges of moving on vertical supports. Unfortunately, these studies are usually limited in scope and do not account for varying strategies based on body size or phylogeny. Here, we test the hypothesis that the spatiotemporal gait characteristics that are used during horizontal walking in primates are also present during vertical climbing irrespective of body size and phylogeny. We examined footfall patterns, diagonality, speed and stride length in eight species of primates across a range of body masses. We found that, during vertical climbing, primates slow down, keep more limbs in contact with the substrate at any one time, and increase the frequency of lateral-sequence gaits compared with horizontal walking. Taken together, these characteristics are assumed to increase stability during locomotion. Phylogenetic relatedness and body size differences have little influence on locomotor patterns observed across species. These data reject the idea that the suite of spatiotemporal gait features observed in primates during horizontal walking are in some way evolutionarily linked to selective pressures associated with mechanical requirements of vertical climbing. These results also highlight the importance of behavioral flexibility for negotiating the challenges of locomotion in an arboreal environment.

Do forelimb shape and peak forces co-vary in strepsirrhines?

OBJECTIVES: In this study, we explore whether ground reaction forces recorded during horizontal walking co-vary with the shape of the long bones of the forelimb in strepsirrhines. To do so, we quantify (1) the shape of the shaft and articular surfaces of each long bone of the forelimb, (2) the peak vertical, mediolateral, and horizontal ground reaction forces applied by the forelimb during arboreal locomotion, and (3) the relationship between the shape of the forelimb and peak forces. MATERIALS AND METHODS: Geometric morphometric approaches were used to quantify the shape of the bones. Kinetic data were collected during horizontal arboreal walking in eight species of strepsirrhines that show variation in habitual substrate use and morphology of the forelimb. These data were then used to explore the links between locomotor behavior, morphology, and mechanics using co-variation analyses in a phylogenetic framework. RESULTS: Our results show significant differences between slow quadrupedal climbers (lorises), vertical clinger and leapers (sifaka), and active arboreal quadrupeds (ring-tailed lemur, ruffed lemur) in both ground reaction forces and the shape of the long bones of the forelimb, with the propulsive and medially directed peak forces having the highest impact on the shape of the humerus. Co-variation between long bone shape and ground reaction forces was detected in both the humerus and ulna even when accounting for differences in body mass. DISCUSSION: These results demonstrate the importance of considering limb-loading beyond just peak vertical force, or substrate reaction force. A re-evaluation of osseous morphology and functional interpretations is necessary in light of these findings.

Inter-stride variability triggers gait transitions in mammals and birds.

Speed-related gait transitions occur in many animals, but it remains unclear what factors trigger gait changes. While the most widely accepted function of gait transitions is that they reduce locomotor costs, there is no obvious metabolic trigger signalling animals when to switch gaits. An alternative approach suggests that gait transitions serve to reduce locomotor instability. While there is evidence supporting this in humans, similar research has not been conducted in other species. This study explores energetics and stride variability during the walk-run transition in mammals and birds. Across nine species, energy savings do not predict the occurrence of a gait transition. Instead, our findings suggest that animals trigger gait transitions to maintain high locomotor rhythmicity and reduce unstable states. Metabolic efficiency is an important benefit of gait transitions, but the reduction in dynamic instability may be the proximate trigger determining when those transitions occur.

The evolution of vertical climbing in primates: evidence from reaction forces.

Vertical climbing is an essential behavior for arboreal animals, yet limb mechanics during climbing are poorly understood and rarely compared with those observed during horizontal walking. Primates commonly engage in both arboreal walking and vertical climbing, and this makes them an ideal taxa in which to compare these locomotor forms. Additionally, primates exhibit unusual limb mechanics compared with most other quadrupeds, with weight distribution biased towards the hindlimbs, a pattern that is argued to have evolved in response to the challenges of arboreal walking. Here we test an alternative hypothesis that functional differentiation between the limbs evolved initially as a response to climbing. Eight primate species were recorded locomoting on instrumented vertical and horizontal simulated arboreal runways. Forces along the axis of, and normal to, the support were recorded. During walking, all primates displayed forelimbs that were net braking, and hindlimbs that were net propulsive. In contrast, both limbs served a propulsive role during climbing. In all species, except the lorisids, the hindlimbs produced greater propulsive forces than the forelimbs during climbing. During climbing, the hindlimbs tends to support compressive loads, while the forelimb forces tend to be primarily tensile. This functional disparity appears to be body-size dependent. The tensile loading of the forelimbs versus the compressive loading of the hindlimbs observed during climbing may have important evolutionary implications for primates, and it may be the case that hindlimb-biased weight support exhibited during quadrupedal walking in primates may be derived from their basal condition of climbing thin branches.

Crouching to fit in: the energetic cost of locomotion in tunnels.

Animals that are specialized for a particular habitat or mode of locomotion often demonstrate locomotor efficiency in a focal environment when compared to a generalist species. However, measurements of these focal habitats or behaviors are often difficult or impossible to do in the field. In this study, the energetics and kinematics of simulated tunnel locomotion by two unrelated semi-fossorial mammals, the ferret and degu, were analyzed using open-flow respirometry and digital video. Animals were trained to move inside of normal (unconstrained, overground locomotion) and height-decreased (simulated tunnel, adjusted to tolerance limits for each species) Plexiglas chambers that were mounted flush onto a treadmill. Both absolute and relative tunnel performance differed between the species; ferrets tolerated a tunnel height that forced them to crouch at nearly 25% lower hip height than in an unconstrained condition, whereas degus would not perform on the treadmill past a ∼9% reduction in hip height. Both ferrets and degus exhibited significantly higher metabolic rates and cost of transport (CoT) values when moving in the tunnel condition relative to overground locomotion. When comparing CoT values across small (<10 kg) mammals, ferrets demonstrated a lower than predicted metabolic cost during both tunnel and terrestrial locomotion, whereas degus were very close to the line of best fit. Although tunnel locomotion requires a more striking change in posture for ferrets, ferrets are more efficient locomotors in both conditions than mammals of similar mass.

Self-Reported Minimalist Running Injury Incidence and Severity: A Pilot Study.

INTRODUCTION: Minimalist running entails using shoes with a flexible thin sole and is popular in the United States. Existing literature disagrees over whether minimalist running shoes (MRS) improve perceived severity of injuries associated with running in traditional running shoes (TRS). Additionally, the perceived injury patterns associated with MRS are relatively unknown. OBJECTIVES: To examine whether injury incidence and severity (ie, degree of pain) by body region change after switching to MRS, and to determine if transition times affect injury incidences or severity with MRS. METHODS: Runners who were either current or previous users of MRS were recruited to complete an Internet-based survey regarding self-reported injury before switching to MRS and whether self-reported pain from that injury decreased after switching. Questions regarding whether new injuries developed in respondents after switching to MRS were also included. Analyses were calculated using t tests, Wilcoxon signed rank tests, and Fischer exact tests. RESULTS: Forty-seven runners completed the survey, and 16 respondents reported injuries before switching to MRS. Among these respondents, pain resulting from injuries of the feet (P=.03) and knees (P=.01) decreased. Eighteen respondents (38.3%) indicated they sustained new injuries after switching to MRS, but the severity of these did not differ significantly from no injury. Neither time allowed for transition to MRS nor use or disuse of a stretching routine during this period was correlated with an increase in the incidence or severity of injuries. CONCLUSION: After switching to MRS, respondents perceived an improvement in foot and knee injuries. Additionally, respondents using MRS reported an injury rate of 38.3%, compared with the approximately 64% that the literature reports among TRS users. Future studies should be expanded to determine the full extent of the differences in injury patterns between MRS and TRS.

Single-limb force data for two lemur species while vertically clinging.

OBJECTIVES: Vertical clinging and climbing have been integral to hypotheses about primate origins, yet little is known about how an animal with nails instead of claws resists gravity while on large, vertical, and cylindrical substrates. Here we test models of how force is applied to maintain posture, predicting (1) the shear component force (Fs ) at the hands will be higher than the feet; (2) the normal component force (Fn ) at the feet will be relatively high compared to the hands; (3) the component force resisting gravity (Fg ) at the feet will be relatively high compared to the hands; (4) species with a high frequency of vertical clinging postures will have low Fg at the hands due to relatively short forelimbs. MATERIALS AND METHODS: Using a novel instrumented support, single-limb force data were collected during clinging postures for the hands and feet and compared across limbs and species for Propithecus verreauxi (N = 2), a habitual vertical clinger and leaper, and Varecia variegata (N = 3), a habitual above-branch arboreal quadruped. RESULTS: For both species, hand Fs were significantly higher than at the feet and Fn and Fg at the feet were significantly higher than at the hands. Between species, P. verreauxi has relatively low Fg at the hands and Fn at the feet than V. vareigata. DISCUSSION: These results support previous models and show that hindlimb loading dominance, characteristic of primate locomotion, is found during clinging behaviors and may allow the forelimbs to be used for foraging while clinging. These findings provide insight into selective pressures on force distribution in primates and primate locomotor evolution.

Kinetics of bipedal locomotion during load carrying in capuchin monkeys.

Facultative bipedalism during load transport in nonhuman primates has been argued to be an important behavior potentially leading to the evolution of obligate, extended limb bipedalism. Understanding the biomechanics of such behavior may lead to insights about associated morphology, which may translate to interpretation of features in the fossil record. Some populations of bearded capuchin monkeys (Sapajus libidinosus) spontaneously carry heavy loads bipedally during foraging activities. This study provides the first data on all three components of ground reaction force for spontaneous bipedalism during load carriage in a nonhuman primate. Five individual S. libidinosus (mean body mass = 2.4 kg ± 0.96) were videorecorded during bipedalism while carrying a stone (0.93 kg) under natural conditions. A force plate was embedded in the path of the monkeys. Spatiotemporal and force data for all three components of the ground reaction force were recorded for 28 steps. Capuchins exhibited a mean vertical peak force per total weight (Vpk) for the hindlimb of 1.19 (sd = 0.13), consistent with those of unloaded capuchins in the laboratory and for other bipedal primates, including humans. Vertical force records suggest that capuchins, along with most nonhuman primates, maintain a relatively compliant leg during both unloaded and loaded locomotion. Like all other primates, loaded capuchins maintained laterally (outward) directed medio-lateral forces, presumably to stabilize side-to-side movements of the center of mass. Medio-lateral forces suggest that at near-running speeds dynamic stability diminishes the need to generate high lateral forces. Vertical force traces exhibited a measurable impact spike at foot contact in 85% of the steps recorded. An impact spike is common in human walking and running but has not been reported in other bipedal primates. This spike in humans is thought to lead to bone and cartilage damage. The earliest biped may have experienced similar impact spikes during bipedal locomotion, requiring compensatory behaviors or anatomical features.

Lower extremity biomechanical relationships with different speeds in traditional, minimalist, and barefoot footwear.

Minimalist running footwear has grown increasingly popular. Prior studies that have compared lower extremity biomechanics in minimalist running to traditional running conditions are largely limited to a single running velocity. This study compares the effects of running at various speeds on foot strike pattern, stride length, knee angles and ankle angles in traditional, barefoot, and minimalist running conditions. Twenty-six recreational runners (19-46 years of age) ran on a treadmill at a range of speeds (2.5-4.0 m·sec(-1)). Subjects ran with four different footwear conditions: personal, standard, and minimalist shoes and barefoot. 3D coordinates from video data were collected. The relationships between speed, knee and ankle angles at foot strike and toe-off, relative step length, and footwear conditions were evaluated by ANCOVA, with speed as the co-variate. Distribution of non-rearfoot strike was compared across shod conditions with paired t-tests. Non-rearfoot strike distribution was not significantly affected by speed, but was different between shod conditions (p < 0.05). Footwear condition and speed significantly affected ankle angle at touchdown, independent of one another (F [3,71] = 10.28, p < 0.001), with barefoot and minimalist running exhibiting greater plantarflexion at foot strike. When controlling for foot strike style, barefoot and minimalist runners exhibited greater plantarflexion than other conditions (p < 0.05). Ankle angle at lift-off and relative step length exhibited a significant interaction between speed and shod condition. Knee angles had a significant relationship with speed, but not with footwear. There is a clear influence of footwear, but not speed, on foot strike pattern. Additionally, speed and footwear predict ankle angles (greater plantarflexion at foot strike) and may have implications for minimalist runners and their risk of injury. Long-term studies utilizing various speeds and habituation times are needed. Key pointsFoot strike style does not change with speed, but does change with shod condition, with minimalist shoes exhibiting an intermediate distribution of forefoot strikes between barefoot and traditional shoes.Plantarflexion at touchdown does change with speed and with shoe type, with barefoot and minimalist shoes exhibiting a greater plantarflexion angle than traditional running shoes.Knee angles change with speed in all shod conditions, but knee flexion at touchdown is not different between shod conditions.Relative step length changes with speed and shod condition, but there is an interaction between these variables such that step length increases more quickly in traditional shoes as speed increases.

Kinematics of bipedal locomotion while carrying a load in the arms in bearded capuchin monkeys (Sapajus libidinosus).

Understanding the selective pressures that drove the evolution of bipedalism in the human lineage may help inform researchers about the locomotor mode(s) of pre-hominin ancestors. Several selective pressures have been hypothesized, including the need to carry food, tools, or infants. Bearded capuchin monkeys are an excellent primate in which to examine the hypothesis that carrying supported the evolution of bipedalism because they are morphologically generalized and in some ways similar to Miocene hominoids, from which the transitional biped evolved. Additionally, bearded capuchins regularly move bipedally while carrying tools that represent a significant portion of their body mass. Here, we examined the spatio-temporal and kinematic gait parameters in a wild setting of Sapajus libidinosus moving bipedally while carrying a stone tool, as well as unloaded bipedal tufted capuchins in the lab. Results indicate that compared with humans, the monkeys move with a more bent-hip, bent-knee posture during both types of bipedalism, as expected. Few differences exist in spatio-temporal or kinematic parameters within species across load-carrying and unloaded bipedalism. The capuchin ankle, however, during load-carrying goes through a greater range of motion in relatively less time than both humans and unloaded capuchins. Data from this study provide the first quantitative data on bipedalism during load-carrying by wild primates in a natural setting. As such, they are a useful comparative reference for understanding bipedalism, particularly during load-carrying.

Locomotor energetics in primates: gait mechanics and their relationship to the energetics of vertical and horizontal locomotion.

All primates regularly move within three-dimensional arboreal environments and must often climb, but little is known about the energetic costs of this critical activity. Limited previous work on the energetics of incline locomotion suggests that there may be differential selective pressures for large compared to small primates in choosing to exploit a complex arboreal environment. Necessary metabolic and gait data have never been collected to examine this possibility and biomechanical mechanisms that might explain size-based differences in the cost of arboreal movement. Energetics and kinematics were collected for five species of primate during climbing and horizontal locomotion. Subjects moved on a treadmill with a narrow vertical substrate and one with a narrow horizontal substrate at their maximum sustainable speed for 10­20 min while oxygen consumption was monitored. Data during climbing were compared to those during horizontal locomotion and across size. Results show that climbing energetic costs were similar to horizontal costs for small primates (<0.5 kg) but were nearly double for larger species. Spatio-temporal gait characteristics suggest that the relationship between the cost of locomotion and the rate of force production changes between the two locomotor modes. Thus, the main determinants of climbing costs are fundamentally different from those during horizontal locomotion. These new results combining spatiotemporal and energetic data confirm and expand on our previous argument (Hanna et al.: Science 320 (2008) 898) that similar costs of horizontal and vertical locomotion in small primates facilitated the successful occupation of a fine-branch arboreal milieu by the earliest primates.

Comparative triceps surae morphology in primates: a review.

Primate locomotor evolution, particularly the evolution of bipedalism, is often examined through morphological studies. Many of these studies have examined the uniqueness of the primate forelimb, and others have examined the primate hip and thigh. Few data exist, however, regarding the myology and function of the leg muscles, even though the ankle plantar flexors are highly important during human bipedalism. In this paper, we draw together data on the fiber type and muscle mass variation in the ankle plantar flexors of primates and make comparisons to other mammals. The data suggest that great apes, atelines, and lorisines exhibit similarity in the mass distribution of the triceps surae. We conclude that variation in triceps surae may be related to the shared locomotor mode exhibited by these groups and that triceps surae morphology, which approaches that of humans, may be related to frequent use of semiplantigrade locomotion and vertical climbing.

The energetic cost of climbing in primates.

Primates are exceptional among mammals for their climbing abilities and arboreal lifestyles. Here we show that small primates (less than 0.5 kilogram) consume the same amount of mass-specific energy (COTTOT) whether climbing or walking a given distance. COTTOT decreases with increasing body size for walking but does not change for climbing. This divergence of COTTOT is likely due to fundamental differences in the biomechanical determinants of the costs of climbing versus walking. These results have important implications for understanding the origins of primates, suggesting that small early primates may have been able to move into a novel arboreal niche without increasing metabolic costs.

Adaptive value of ambling gaits in primates and other mammals.

At speeds between the walk and the gallop, most mammals trot. Primates almost never trot, and it has been claimed that they transition directly from a walk to a gallop without any distinctive mid-speed running gait. If true, this would be another characteristic difference between the locomotion of primates and that of most other quadrupedal mammals. Presently, however, few data exist concerning the actual presence or absence of intermediate-speed gaits (i.e. gaits that are used between a walk and a gallop) in primates. Video records of running in twelve primate species reveal that, unlike most other mammals, all the primates studied almost exclusively adopt an 'amble'--an intermediate-speed running gait with no whole-body aerial phase--rather than trot. Ambling is also common in elephants and some horses, raising the question of why ambling is preferred over trotting in these diverse groups of animals. Mathematical analyses presented here show that ambling ensures continuous contact of the body with the substrate while dramatically reducing vertical oscillations of the center of mass. This may explain why ambling appears to be preferable to trotting for extremely large terrestrial mammals such as elephants and for arboreal mammals like primates that move on unstable branches. These findings allow us to better understand the mechanics of these unusual running gaits and shed new light on primate locomotor evolution.

Molar scaling in strepsirrhine primates.

We examined how maxillary molar dimensions change with body and skull size estimates among 54 species of living and subfossil strepsirrhine primates. Strepsirrhine maxillary molar areas tend to scale with negative allometry, or possibly isometry, relative to body mass. This observation supports several previous scaling analyses showing that primate molar areas scale at or slightly below geometric similarity relative to body mass. Strepsirrhine molar areas do not change relative to body mass(0.75), as predicted by the metabolic scaling hypothesis. Relative to basicranial length, maxillary molar areas tend to scale with positive allometry. Previous claims that primate molar areas scale with positive allometry relative to body mass appear to rest on the incorrect assumption that skull dimensions scale isometrically with body mass. We identified specific factors that help us to better understand these observed scaling patterns. Lorisiform and lemuriform maxillary molar scaling patterns did not differ significantly, suggesting that the two infraorders had little independent influence on strepsirrhine scaling patterns. Contrary to many previous studies of primate dental allometry, we found little evidence for significant differences in molar area scaling patterns among frugivorous, folivorous, and insectivorous groups. We were able to distinguish folivorous species from frugivorous and insectivorous taxa by comparing M1 lengths and widths. Folivores tend to have a mesiodistally elongated M1 for a given buccolingual M1 width when compared to the other two dietary groups. It has recently been shown that brain mass has a strong influence on primate dental eruption rates. We extended this comparison to relative maxillary molar sizes, but found that brain mass appears to have little influence on the size of strepsirrhine molars. Alternatively, we observed a strong correlation between the relative size of the facial skull and relative molar areas among strepsirrhines. We hypothesize that this association may be underlain by a partial sharing of the patterning of development between molar and facial skull elements.

Substrate alters forelimb to hindlimb peak force ratios in primates.

It is often claimed that the walking gaits of primates are unusual because, unlike most other mammals, primates appear to have higher vertical peak ground reaction forces on their hindlimbs than on their forelimbs. Many researchers have argued that this pattern of ground reaction force distribution is part of a general adaptation to arboreal locomotion. This argument is frequently used to support models of primate locomotor evolution. Unfortunately, little is known about the force distribution patterns of primates walking on arboreal supports, nor do we completely understand the mechanisms that regulate weight distribution in primates. We collected vertical peak force data for seven species of primates walking quadrupedally on instrumented terrestrial and arboreal supports. Our results show that, when walking on arboreal vs. terrestrial substrates, primates generally have lower vertical peak forces on both limbs but the difference is most extreme for the forelimb. We found that force reduction occurs primarily by decreasing forelimb and, to a lesser extent, hindlimb stiffness. As a result, on arboreal supports, primates experience significantly greater functional differentiation of the forelimb and hindlimb than on the ground. These data support long-standing theories that arboreal locomotion was a critical factor in the differentiation of the forelimbs and hindlimbs in primates. This change in functional role of the forelimb may have played a critical role in the origin of primates and facilitated the evolution of more specialized locomotor behaviors.