Behavioral implications of ontogenetic changes in intrinsic hand and foot proportions in olive baboons (Papio Anubis).

OBJECTIVES: Relatively long digits are considered to enhance grasping performance in primates. We tested whether growth-related changes in intrinsic hand and foot proportions may have behavioral implications for growing animals, by examining whether ontogenetic changes in digital proportions are related to variation in voluntary grasping behaviors in baboons. MATERIALS AND METHODS: Longitudinal morphological and behavioral data were collected on 6 captive olive baboons (Papio anubis) as they aged from 5 to 22 months. The length of digits and metapodials, measured from radiographs, were used to calculate phalangeal indices (i.e., PIs: summed length of non-distal phalanges relative to corresponding metapodial length). We also examined the allometric scaling of digital bones relative to body mass. We observed baboon positional behaviors over a 15-day period following the radiographic sessions, quantifying the frequency of forelimb and hindlimb grasping behaviors. RESULTS: PIs for all digits declined during growth, a result of the differential scaling of metapodials (which scaled to body mass with isometry) versus phalanges (which scaled with negative allometry). The incidence of forelimb and hindlimb grasping behaviors declined with age. Though we found no relationship between forelimb grasping and hand proportions, the incidence of hindlimb grasping was directly correlated with postaxial digit PIs. DISCUSSION: Only changes in the intrinsic proportions of the pedal digits are associated with variation in grasping activity in growing baboons. This finding accords previous biomechanical and neuroanatomical studies showing distinct functional roles for the hands and feet during primate locomotion, and has important implications for reconstructing primate locomotor evolution.

Wavy multistratified amacrine cells in the monkey retina contain immunoreactive secretoneurin.

The goals of this study were to describe the morphology, neurotransmitter content and synaptic connections of neurons in primate retinas that contain the neuropeptide secretoneurin. Amacrine cells were labeled with antibodies to secretoneurin in macaque and baboon retinas. Their processes formed three distinct plexuses in the inner plexiform layer: one in the outermost stratum, one in the center and one in the innermost stratum. In light microscopic double immunolabeling experiments, GABA was colocalized with secretoneurin in these cells, but glycine transporter 1 and Substance P were not. ON bipolar cell axon terminals labeled with antibody to the cholecystokinin precursor, G6-gly, have ON responses to stimulation of short wavelength sensitive (S) cones. Axons of these bipolar cells made contacts with amacrine cell dendrites containing secretoneurin. Secretoneurin-IR amacrine cells also made contacts with retinal ganglion cell dendrites labeled with antibody to the photopigment melanopsin, which have OFF responses to stimulation of S cones. Using electron microscopic immunolabeling, 436 synapses from macaque retina were analyzed. Axons from bipolar cells were identified by their characteristic synaptic ribbons; their synaptic densities were asymmetric like those of excitatory synapses in the brain. Amacrine cells made and received conventional synapses with symmetric synaptic densities, like those of inhibitory synapses in the brain. Ganglion cell dendrites were identified by their absence of presynaptic specializations; they received inputs from both amacrine cells and bipolar cells. The majority of inputs to the secretoneurin-IR amacrine cells were from other amacrine cells, but they also received 21% of their input from bipolar cells. They directed most of their output, 54%, to amacrine cells, but there were many synapses onto bipolar cell axons and ganglion cell dendrites, as well. The synaptic connections were very similar in the three plexuses with one notable exception; output synapses to bipolar cells were significantly less common in the innermost one, where the S-ON bipolar cells terminate. Taken together, these findings suggest that the secretoneurin-IR amacrine cells in primates receive excitatory input from S-ON bipolar cells and, in turn, inhibit intrinsically photosensitive retinal ganglion cells.

Age-associated remodeling of the intestinal epithelial barrier.

Disorders of the gastrointestinal tract are common in the elderly people; however, the precise trait(s) of aging that contribute to the vulnerability of the gastrointestinal tract are poorly understood. Recent evidence suggests that patients with gastrointestinal disorders have increased intestinal permeability. Here, we address the hypothesis that disruption of the intestinal barrier is associated with aging. Our results demonstrated that permeability was significantly higher in colonic biopsies collected from old baboons compared with young baboons. Additionally, colonic tissue from the older animals had decreased zonula occluden-1, occludin, and junctional adhesion molecule-A tight junction protein expression and increased claudin-2 expression. Upregulation of miR-29a and inflammatory cytokines IFN-γ, IL-6, and IL-1ß was also found in colonic biopsies from old baboons relative to young baboons. These results show for the first time that a pivotal contributing factor to geriatric vulnerability to gastrointestinal dysfunction may be increased colonic permeability via age-associated remodeling of intestinal epithelial tight junction proteins.

Electromyography of wrist and finger flexor muscles in olive baboons (Papio anubis).

Some non-human primates use digitigrade hand postures when walking slowly on the ground. As a component of an extended limb, a digitigrade posture can help minimize wrist joint moments thereby requiring little force production directly from wrist flexors (and/or from the assistance of finger flexors) to maintain limb posture. As a consequence, less active muscle volume would be required from these anti-gravity muscles and overall metabolic costs associated with locomotion could be reduced. To investigate whether the use of digitigrade hand postures during walking in primates entails minimal use of anti-gravity muscles, this study examined electromyography (EMG) patterns in both the wrist and finger flexor muscles in facultatively digitigrade olive baboons (Papio anubis) across a range of speeds. The results demonstrate that baboons can adopt a digitigrade hand posture when standing and moving at slow speeds without requiring substantial EMG activity from distal anti-gravity muscles. Higher speed locomotion, however, entails increasing EMG activity and is accompanied by a dynamic shift to a more palmigrade-like limb posture. Thus, the ability to adopt a digitigrade hand posture by monkeys is an adaptation for ground living, but it was never co-opted for fast locomotion. Rather, digitigrady in primates appears to be related to energetic efficiency for walking long distances.

Healthy baboon with no upper jaw or nose: an extreme case of adaptability in the Kibale National Park, Uganda.

We describe and document with digital images an adult female baboon (Papio anubis) from the Kibale National Park, Uganda, who was missing all but the basal part of her upper jaw and nose, i.e., no premaxilla and very little of the maxilla and nasal bones. She appeared otherwise healthy, well integrated into a social group, and apparently reproducing, based on the fact that she was grooming a juvenile who suckled from her and that she appeared to be pregnant. Her extreme deformity raises numerous questions and demonstrates the highly adaptable capabilities of wild baboons.

Dynamic pressure patterns in the hands of olive baboons (Papio anubis) during terrestrial locomotion: implications for cercopithecoid primate hand morphology.

Habitually terrestrial monkeys adopt digitigrade hand postures at slow speeds to increase effective forelimb length and reduce distal limb joint moments. As these primates move faster, however, their hands transition to a more palmigrade posture, which is likely associated with the inability of wrist and hand joints to resist higher ground reaction forces (GRF) associated with faster speeds. Transitioning to a palmigrade posture may serve to distribute GRFs over a larger surface area (i.e., increased palmar contact), ultimately reducing stresses in fragile hand bones. To test this hypothesis, dynamic palmar pressure data were collected on two adult baboons (Papio anubis) walking, running, and galloping across a runway integrated with a dynamic pressure mat (20 steps each; speed range: 0.46-4.0 m/s). Peak GRF, contact area, peak pressure, and pressure-time integral were quantified in two regions of the hand: fingers and palms (including metacarpal heads). At slower speeds with lower GRFs, the baboons use digitigrade postures resulting in small palmar contact area (largely across the metacarpal heads). At faster speeds with higher GRFs, they used less digitigrade hand postures resulting in increased palmar contact area. Finger contact area did not change across speeds. Despite higher GRFs at faster speeds, metacarpal pressure was moderated across speeds due to increased palmar contact area as animals transitioned from digitigrady to palmigrady. In contrast, the pressure in the fingers increased with faster speeds. Results indicate that the transition from digitigrady to palmigrady distributes increased forces over a larger palmar surface area. Such dynamic changes in palmar pressure likely moderate strain in the gracile bones of the hand, a structure that is integral not only for locomotion, but also feeding and social behaviors in primates.

Not so fast: speed effects on forelimb kinematics in cercopithecine monkeys and implications for digitigrade postures in primates.

Terrestrial mammals are characterized by their digitigrade limb postures, which are proposed to increase effective limb length (ELL) to achieve preferred or higher locomotor speeds more efficiently. Accordingly, digitigrade postures are associated with cursorial locomotion. Unlike most medium- to large-sized terrestrial mammals, terrestrial cercopithecine monkeys lack most cursorial adaptations, but still adopt digitigrade hand postures. This study investigates when and why terrestrial cercopithecine monkeys adopt digitigrade hand postures during quadrupedal locomotion. Three cercopithecine species (Papio anubis, Macaca mulatta, Erythrocebus patas) were videotaped moving unrestrained along a horizontal runway at a range of speeds (0.4-3.4 m/s). Three-dimensional forelimb kinematic data were recorded during forelimb support. Hand posture was measured as the angle between the metacarpal segments and the ground (MGA). As predicted, a larger MGA was correlated with a longer ELL. At slower speeds, subjects used digitigrade postures (larger MGA), however, contrary to expectations, all subjects used more palmigrade hand postures (smaller MGA) at faster speeds. Digitigrade postures at slower speeds may lower cost of transport by increasing ELL and step lengths. At higher speeds, palmigrade postures may be better suited to spread out high ground reaction forces across a larger portion of the hand thereby potentially decreasing stresses in hand bones. It is concluded that a digitigrade forelimb posture in primates is not an adaptation for high speed locomotion. Accordingly, digitigrady may have evolved for different reasons in primates compared to other mammalian lineages.

The femoral artery and its branches in the baboon Papio anubis.

The aim of the research was to examine the anatomy of the arterial system in the inguinal region, hip and thigh of Papio anubis. No description of this was found in the available scientific literature, although, at the same time, the baboon is considered to be a good animal model in biomedical research. Macroscopic anatomical research was carried out on 20 hind limbs (10 cadavers: 9 male and 1 female) of adult Papio anubis and the results were then compared with the anatomy of the arterial hind limb systems of other apes as described in the literature. The circulatory system of the whole body was filled with coloured latex via the common carotid artery and internal jugular vein, and traditional methods were then used to prepare the vessels. The arterial system in the hind extremity of Papio anubis was recorded. The anatomical names of human arteries were used as well as the names of those of apes as applied in the literature. The femoral artery was the only artery supplying the hind limb of Papio anubis. It started under the inguinal ligament as a continuation of the external iliac artery. It went down and divided into the popliteal artery, which coursed in the popliteal fossa, and the saphenous artery, which passed on the medial side of the thigh and leg. The number of smaller branches and the way in which they issued from the larger arteries were documented. The external diameter and length of the hind limb arteries were measured. It was observed that the cutaneous branches of the femoral artery supplied the inguinal and genital regions and the abdominal wall, while the deep artery of the thigh was the main vessel of the hip and thigh.

Assessment of buprenorphine, carprofen, and their combination for postoperative analgesia in olive baboons (Papio anubis).

This study compared the efficacy of buprenorphine, carprofen, and a combination of the 2 analgesics in female baboons. Physiologic and behavioral parameters were assessed at baseline and postoperatively for 6 d by use of continuous noninvasive physiologic monitoring and twice-daily videotaping. Prior to surgery, all animals received a pre-emptive dose of either 0.01 mg/kg buprenorphine intramuscularly, 2.2 mg/kg carprofen intramuscularly, or a combination of 0.01 mg/kg buprenorphine and 2.2 mg/kg carprofen intramuscularly. All animals in the carprofen (n = 4) and buprenorphine+carprofen (n = 4) treatment groups appeared to have sufficient analgesia. Three of 4 animals in the buprenorphine group had adequate analgesia. The fourth animal had an elevated heart rate and spent less time standing during the postoperative period. In this study, the use of carprofen or a combination of carprofen plus buprenorphine provided more reliable postoperative analgesia than buprenorphine alone.

Superficial veins of the foot in the baboon Papio anubis.

Although the baboon is considered a good animal model in biomedical research, no description of the superficial veins of the foot in Papio anubis is found in the available literature. The current study was conducted to document the anatomy of these veins in the baboon foot. A macroscopic anatomical investigation was carried out on 20 hind legs (10 cadavers) of the adult Papio anubis (9 males and 1 female). The circulatory system of the entire body was filled with coloured latex. Traditional methods were used for the preparation of the veins of the legs. These were then compared with the venous system of the lower extremities in humans as presented in the literature. The medial and lateral metatarsal veins, the dorsal venous network, the long saphenous vein and the short saphenous vein in Papio anubis were described according to their origin, course, opening, length and diameter. The network observed was divided into three types with respect to the connections between the superficial veins. The investigation revealed no symmetry in the venous system of the baboon foot. The short saphenous vein appeared to be the main vein of the hind leg in Papio anubis and the long saphenous vein ran as a double vessel.

Phase II jaw movements and masseter muscle activity during chewing in Papio anubis.

It was proposed that the power stroke in primates has two distinct periods of occlusal contact, each with a characteristic motion of the mandibular molars relative to the maxillary molars. The two movements are called phase I and phase II, and they occur sequentially in that order (Kay and Hiiemae [1974] Am J. Phys. Anthropol. 40:227-256, Kay and Hiiemae [1974] Prosimian Biology, Pittsburgh: University of Pittsburgh Press, p. 501-530). Phase I movement is said to be associated with shearing along a series of crests, producing planar phase I facets and crushing on surfaces on the basins of the molars. Phase I terminates in centric occlusion. Phase II movement is said to be associated with grinding along the same surfaces that were used for crushing at the termination of phase I. Hylander et al. ([1987] Am J. Phys. Anthropol. 72:287-312; see also Hiiemae [1984] Food Acquisition and Processing, London: Academic Press, p. 257-281; Hylander and Crompton [1980] Am J. Phys. Anthropol. 52:239-251, [1986] Arch. Oral. Biol. 31:841-848) analyzed data on macaques and suggested that phase II movement may not be nearly as significant for food breakdown as phase I movement simply because, based on the magnitude of mandibular bone strain patterns, adductor muscle and occlusal forces are likely negligible during movement out of centric occlusion. Our goal is to better understand the functional significance of phase II movement within the broader context of masticatory kinematics during the power stroke. We analyze vertical and transverse mandibular motion and relative activity of the masseter and temporalis muscles during phase I and II movements in Papio anubis. We test whether significant muscle activity and, by inference, occlusal force occurs during phase II movement. We find that during phase II movement, there is negligible force developed in the superficial and deep masseter and the anterior and posterior temporalis muscles. Furthermore, mandibular movements are small during phase II compared to phase I. These results suggest that grinding during phase II movement is of minimal importance for food breakdown, and that most food breakdown on phase II facets occurs primarily at the end of phase I movement (i.e., crushing during phase I movement). We note, however, that depending on the orientation of phase I facets, significant grinding also occurs along phase I facets during phase I.

The topography of the superficial veins of the hind leg in the baboon Papio anubis in comparison with the superficial veins of the lower limb in humans.

Our studies were carried out on 8 male and 2 female baboons Papio anubis cadavers. We examined a total of 20 hind legs. The vessels of the hind leg were filled with coloured latex. Afterwards we prepared the superficial and deep veins and accompanying arteries. We paid attention to the location, diameter and the course of the long and short saphenous veins. We found many differences between the system of superficial veins in the baboon hind leg and that in the human lower limb. First of all, the long saphenous vein in the baboon Papio anubis presented as two similar trunks that ran together with a concomitant artery. The saphenofemoral junction was also duplicated. The distance between these outlets was about 4 mm and their location was different from that in humans. Neither trunk exceeded 2.5 m in diameter. Some human-like features were noticed in the system of the short saphenous vein in Papio anubis. The diameter of the short saphenous vein and its course and the location of the saphenopopliteal junction were very similar to those in humans. On the other hand, the short saphenous vein was the main superficial venous channel of the hind limb of Papio anubis.

Dental microwear in anubis and hybrid baboons (Papio hamadryas, sensu lato) living in Awash National Park, Ethiopia.

We describe dental microwear in baboons (Papio hamadryas sensu lato) from the anubis-hamadryas hybrid zone of Awash National Park, Ethiopia, outline its variation with sex and age, and attempt to relate the observed microwear pattern to environment and diet. Casts of the maxillary second molar of 52 adult and subadult individuals of both sexes were examined with a scanning electron microscope at x 500. Digitized micrographs were taken at a consistent location on facet 9, and microwear was recorded with an image analysis software package. Univariate and multivariate statistics were used to investigate the shape, size, and density of microwear features. The overall pattern of microwear exhibits an unusual combination of high feature density, with numerous small pits and relatively wide striations, and a high correlation between width of pits and striations across individuals. We interpret this pattern as predominantly the consequence of abrasion by relatively small-caliber environmental grit when accidentally ingested with tough foods such as dried seeds and fruits, as expected in a terrestrial omnivore living in a dusty habitat. Statistical analysis revealed no significant differences between groups defined by sex, age, or troop membership, a result consistent with qualitative observations of feeding habits in this population, and which lends no support to the hypothesis that the longer jaws of adult males should result in longer striations. A trend towards greater feature density in females, however, might be due to limited sexual dinichism, and merits further investigation.