Age and sex associated organ weight differences in vervets/African green monkeys (Chlorocebus aethiops sabaeus).

BACKGROUND: African green monkeys (AGMs, also known as vervets, Cholorocebus aethiops sabaeus) have been used in a variety of biomedical research studies. The aim of this study was to generate a reference for normal organ weights and percentage organ weights in AGMs of different age categories and sex. METHODS: The organ weights were compiled from 479 AGMs (285 females and 194 males) from 2004 to 2021. Age and sex differences of absolute and relative organ weights were analyzed using analysis of variance. RESULTS: The findings demonstrate that males had higher body and organ weights than age­matched females, but relative organ weights did not differ between males and females. At maturity, adrenal gland, brain, kidney, liver, thymus, and thyroid gland weights as a percentage of body weight declined, but relative weights of prostate gland, testes, and uterus were higher. CONCLUSION: These data should be beneficial to biomedical researchers and pathologists working with AGMs.

Field data confirm the ability of a biophysical model to predict wild primate body temperature.

In the face of climate change there is an urgent need to understand how animal performance is affected by environmental conditions. Biophysical models that use principles of heat and mass transfer can be used to explore how an animal's morphology, physiology, and behavior interact with its environment in terms of energy, mass and water balances to affect fitness and performance. We used Niche Mapper™ (NM) to build a vervet monkey (Chlorocebus pygerythrus) biophysical model and tested the model's ability to predict core body temperature (Tb) variation and thermal stress against Tb and behavioral data collected from wild vervets in South Africa. The mean observed Tb in both males and females was within 0.5 °C of NM's predicted Tbs for 91% of hours over the five-year study period. This is the first time that NM's Tb predictions have been validated against field data from a wild endotherm. Overall, these results provide confidence that NM can accurately predict thermal stress and can be used to provide insight into the thermoregulatory consequences of morphological (e.g., body size, shape, fur depth), physiological (e.g. Tb plasticity) and behavioral (e.g., huddling, resting, shade seeking) adaptations. Such an approach allows users to test hypotheses about how animals adapt to thermoregulatory challenges and make informed predictions about potential responses to environmental change such as climate change or habitat conversion. Importantly, NM's animal submodel is a general model that can be adapted to other species, requiring only basic information on an animal's morphology, physiology and behavior.

The relative efficacy of the cranium and os coxa for taxonomic assessment in macaques.

OBJECTIVES: The cranium is generally considered more reliable than the postcranium for assessing primate taxonomy, although recent research suggests that pelvic shape may be equally reliable. However, little research has focused on intrageneric taxonomic discrimination. Here, we test the relative taxonomic efficacy of the cranium and os coxa for differentiating two macaque species, with and without considering sexual dimorphism. MATERIALS AND METHODS: Geometric morphometric analyses were performed on cranial and os coxa landmarks for 119 adult Macaca fascicularis, M. mulatta, and Chlorocebus pygerythrus. Among-group shape variation was examined using canonical variates analyses. Cross-validated discriminant function analysis provided rates of correct group classification. Additionally, average morphological distances were compared with neutral genetic distances. RESULTS: Macaque species were clearly differentiated, both cranially and pelvically, when sex was not considered. Males were more often correctly classified based on the os coxa, while female classification rates were high for both morphologies. Female crania and male os coxa were differentiated approximately the same as genetic distance, while male crania were more similar (convergent), and female os coxa were more divergent than expected based on genetic distance. DISCUSSION: The hypothesis that cranial and os coxal shape can be used to discriminate among macaque species was supported. The cranium was better at differentiating females, while the os coxa was better at differentiating male macaques. Hence, there is no a priori reason for preferring the cranium when assessing intragenetic taxonomic relationships, but the effects of high levels of sexual dimorphism must be corrected for to accurately assess taxonomic signatures.

Expression and localization of CB1R, NAPE-PLD, and FAAH in the vervet monkey nucleus accumbens.

Extensive rodent literature suggests that the endocannabinoid (eCB) system present in the nucleus accumbens (NAc) modulates dopamine (DA) release in this area. However, expression patterns of the cannabinoid receptor type 1 (CB1R), the synthesizing enzyme N-acyl phosphatidylethanolamine phospholipase D (NAPE-PLD), and the degradation enzyme fatty acid amide hydrolase (FAAH) in the NAc have not yet been described in non-human primates. The goal of this study is therefore to characterize the expression and localization of the eCB system within the NAc of vervet monkeys (Chlorocebus sabaeus) using Western blots and immunohistochemistry. Results show that CB1R, NAPE-PLD, and FAAH are expressed across the NAc rostrocaudal axis, both in the core and shell. CB1R, NAPE-PLD, and FAAH are localized in medium spiny neurons (MSNs) and fast-spiking GABAergic interneurons (FSIs). Dopaminergic projections and astrocytes did not express CB1R, NAPE-PLD, or FAAH. These data show that the eCB system is present in the vervet monkey NAc and supports its role in the primate brain reward circuit.

Morphological variation in the genus Chlorocebus: Ecogeographic and anthropogenically mediated variation in body mass, postcranial morphology, and growth.

OBJECTIVES: Direct comparative work in morphology and growth on widely dispersed wild primate taxa is rarely accomplished, yet critical to understanding ecogeographic variation, plastic local variation in response to human impacts, and variation in patterns of growth and sexual dimorphism. We investigated population variation in morphology and growth in response to geographic variables (i.e., latitude, altitude), climatic variables (i.e., temperature and rainfall), and human impacts in the vervet monkey (Chlorocebus spp.). METHODS: We trapped over 1,600 wild vervets from across Sub-Saharan Africa and the Caribbean, and compared measurements of body mass, body length, and relative thigh, leg, and foot length in four well-represented geographic samples: Ethiopia, Kenya, South Africa, and St. Kitts & Nevis. RESULTS: We found significant variation in body mass and length consistent with Bergmann's Rule in adult females, and in adult males when excluding the St. Kitts & Nevis population, which was more sexually dimorphic. Contrary to Rensch's Rule, although the South African population had the largest average body size, it was the least dimorphic. There was significant, although very small, variation in all limb segments in support for Allen's Rule. Females in high human impact areas were heavier than those with moderate exposures, while those in low human impact areas were lighter; human impacts had no effect on males. CONCLUSIONS: Vervet monkeys appear to have adapted to local climate as predicted by Bergmann's and, less consistently, Allen's Rule, while also responding in predicted ways to human impacts. To better understand deviations from predicted patterns will require further comparative work in vervets.

Ontogenetic scaling of fore limb and hind limb joint posture and limb bone cross-sectional geometry in vervets and baboons.

OBJECTIVES: Previous studies suggest that the postures habitually adopted by an animal influence the mechanical loading of its long bones. Relatively extended limb postures in larger animals should preferentially reduce anteroposterior (A-P) relative to mediolateral (M-L) bending of the limb bones and therefore decrease A-P/M-L rigidity. We test this hypothesis by examining growth-related changes in limb bone structure in two primate taxa that differ in ontogenetic patterns of joint posture. MATERIALS AND METHODS: Knee and elbow angles of adult and immature vervets (Chlorocebus aethiops, n = 16) were compared to published data for baboons (Papio hamadryas ursinus, n = 33, Patel et al., ). Ontogenetic changes in ratios of A-P/M-L bending rigidity in the femur and humerus were compared in skeletal samples (C. aethiops, n = 28; P. cynocephalus, n = 39). Size changes were assessed with linear regression, and age group differences tested with ANOVA. RESULTS: Only the knee of baboons shows significant postural change, becoming more extended with age and mass. A-P/M-L bending rigidity of the femur decreases during ontogeny in immature and adult female baboons only. Trends in the humerus are less marked. Adult male baboons have higher A-P/M-L bending rigidity of the femur than females. CONCLUSIONS: The hypothesized relationship between more extended joints and reduced A-P/M-L bending rigidity is supported by our results for immature and adult female baboon hind limbs, and the lack of significant age changes in either parameter in forelimbs and vervets. Adult males of both species depart from general ontogenetic trends, possibly due to socially mediated behavioral differences between sexes. Am J Phys Anthropol 161:72-83, 2016. © 2016 Wiley Periodicals, Inc.

Primary bone microanatomy records developmental aspects of life history in catarrhine primates.

A central challenge in human origins research is to understand how evolution has shaped modern human life history. As fossilized remains of our ancestors provide the only direct evidence for life history evolution, efforts to reconstruct life history in paleontological contexts have focused on hard tissues, particularly on dental development. However, among investigators of other vertebrate groups, there is a long tradition of examining primary bone microstructure to decipher growth rates and maturational timing, based on an empirical relationship between the microanatomy of primary bone and the rate at which it is deposited. We examined ontogenetic variation in primary bone microstructure at the midshaft femur of Chlorocebus aethiops, Hylobates lar, and Pan troglodytes to test whether tissue type proportions vary in accordance with predictions based on body mass growth patterns described previously. In all taxa, younger age classes were characterized by significantly higher percent areas of fibro-lamellar and/or parallel-fibered tissues, while older age classes showed significantly higher proportions of lamellar bone. In prior experimental studies, fibro-lamellar and parallel-fibered tissue types have been associated with faster depositional rates than lamellar bone. Principal components analysis revealed differences among taxa in the timing of this transition, and in the particular tissue types observed among individuals of similar dental emergence status. Among M1 and M2 age classes, higher proportions of parallel-fibered and fibro-lamellar tissues were observed in those taxa characterized by reportedly faster body mass growth rates. Further, persistence of fibro-lamellar tissue throughout DECID, M1 and M2 age classes in chimpanzees contrasts with the pattern reported previously for modern humans. Despite the necessary limitations of our cross-sectional study design and the secondary remodeling of bone in primates, large areas of primary bone remain intact and represent a valuable and independent source of information about the evolution of growth and development in the fossil record.

Minor contributions of the maxillary sinus to the air-conditioning performance in macaque monkeys.

The nasal passages mainly adjust the temperature and humidity of inhaled air to reach the alveolar condition required in the lungs. By contrast to most other non-human primates, macaque monkeys are distributed widely among tropical, temperate and subarctic regions, and thus some species need to condition the inhaled air in cool and dry ambient atmospheric areas. The internal nasal anatomy is believed to have undergone adaptive modifications to improve the air-conditioning performance. Furthermore, the maxillary sinus (MS), an accessory hollow communicating with the nasal cavity, is found in macaques, whereas it is absent in most other extant Old World monkeys, including savanna monkeys. In this study, we used computational fluid dynamics simulations to simulate the airflow and heat and water exchange over the mucosal surface in the nasal passage. Using the topology models of the nasal cavity with and without the MS, we demonstrated that the MS makes little contribution to the airflow pattern and the air-conditioning performance within the nasal cavity in macaques. Instead, the inhaled air is conditioned well in the anterior portion of the nasal cavity before reaching the MS in both macaques and savanna monkeys. These findings suggest that the evolutionary modifications and coetaneous variations in the nasal anatomy are rather independent of transitions and variations in the climate and atmospheric environment found in the habitats of macaques.

The endocannabinoid system within the dorsal lateral geniculate nucleus of the vervet monkey.

The endocannabinoid system mainly consists of cannabinoid receptors type 1 (CB1R) and type 2 (CB2R), their endogenous ligands termed endocannabinoids (eCBs), and the enzymes responsible for the synthesis and degradation of eCBs. These cannabinoid receptors have been well characterized in rodent and monkey retinae. Here, we investigated the expression and localization of the eCB system beyond the retina, namely the first thalamic relay, the dorsal lateral geniculate nucleus (dLGN), of vervet monkeys using immunohistochemistry methods. Our results show that CB1R is expressed throughout the dLGN with more prominent labeling in the magnocellular layers. The same pattern is observed for the degradation enzyme, fatty acid amide hydrolase (FAAH). However, the synthesizing enzyme N-acyl-phosphatidylethanolamine phospholipase D (NAPE-PLD) is expressed homogenously throughout the dLGN with no preference for any of the layers. These proteins are weakly expressed in the koniocellular layers. These results suggest that the presence of the eCB system throughout the layers of the dLGN may represent a novel site of neuromodulatory action in normal vision. The larger amount of CB1R in the dLGN magnocellular layers may explain some of the behavioral effects of cannabinoids associated with the integrity of the dorsal visual pathway that plays a role in visual-spatial localization and motion perception.

A model for determining baseline morphometrics of skeletal myofibres.

The minimum diameter method of morphometry (MDM) is used to measure and detect changes in myofibre diameters (FD). The MDM is used to identify pathology in skeletal muscle. In such studies, an assumption is made that the mean FD in a particular muscle in both limbs is essentially the same. This study explored this premise to determine the accuracy of MDM as a means of morphometric analysis. Muscle biopsies were obtained from the left (G1) and right (G2) tibialis anterior of four vervet monkeys and from the massaged left (G3) and untreated right (G4) tibialis anterior of four animals. Wax sections were prepared for MDM and FD was measured. Three specimens were re-measured on four occasions. The mean FD of each biopsy from G1 and G2 limbs were compared and the number of measurements necessary to produce a meaningful result determined. Repeated measurement showed a difference of < 3.0% in FD means between the first and three subsequent measurements. There was no significant difference of FD means between G1 and G2, whilst the difference between G3 and G4 was 11.2%. When > 175 FD were measured, the difference from the final mean was less than 2.0%. These data show that, (1) FD data derived from a muscle in an untreated limb can be used as a control for experiment mediated changes of FD in the other, (2) MDM is a reliable means of measuring FD and (3) 150-175 FD are needed to provide a dependable result.

Thoracic radiographic anatomy in vervet monkeys (Chlorocebus sabaeus).

BACKGROUND: The vervet monkey (Chlorocebus sabaeus) is used commonly in cardiorespiratory biomedical research. This study was performed to establish reference values for thoracic structures and to describe the normal radiographic appearance of the vervet monkey thorax. METHODS: Right lateral and dorsoventral thoracic radiographs of ten mature vervet monkeys were evaluated. Anatomic structures were characterized using descriptive statistics. RESULTS: Normal measurements of skeletal, pulmonary, mediastinal, and cardiovascular structures are reported herein. Several ratios were calculated to assess the cardiac silhouette, caudal vena cava, and pulmonary arteries and veins. CONCLUSIONS: Consistent measurements could be made on the majority of the thoracic structures evaluated. The aorta on lateral radiographs and the pulmonary veins on dorsoventral radiographs were obscured by a mild bronchointerstitial pattern and body conformation. Caudal vena cava-tapering was occasionally noted and attributed to general anesthesia. Species-specific thoracic radiographic reference values should prove useful in vervet monkey disease diagnosis and management.

Myosin heavy chain isoform expression in the Vastus Lateralis muscle of aging African green vervet monkeys.

Non-human primates (NHP) represent an emerging animal model for the study of physical function, and provide opportunities for exploration of relationships of muscle biomolecular changes with age. One such primate model, the African green vervet monkey, has been used extensively in biomedical research but little is known regarding skeletal muscle composition, expression of myosin heavy chain (MHC) isoforms, and changes with age. In the present study we examined the effects of age on vastus lateralis (VL) muscle fiber-type composition, fiber cross-sectional area (CSA), and MHC isoforms expressed in 4 young and 4 older adult vervet monkeys. Proteomics analysis, using a human and nonhuman primate protein database, showed five MHC isoforms (I, IIA, IIX, IIB, and IIB') expressed in female vervet VL muscle, which matched the human MHC isoforms. Fast type II fibers predominated and no pure type IIB or IIB' containing fibers were detected. Hybrid fibers containing IIB/IIB' MHC decreased in the old vervets. The CSA of both type I and type II fibers was significantly smaller in older vervet while type IIA fibers showed the most severity of atrophy. The decrease of fast MHC and atrophy of muscle fiber with aging recapitulate observations in human VL muscle. These findings, along with its homology of MHC between the vervet and human suggested that the vervet monkey may be a suitable preclinical model for understanding the cellular and molecular basis of sarcopenia and for developing new interventions to ameliorate the impact of disorders that affect skeletal muscle structure and function.

Comparison of fresh to fixed weights of the vervet monkey (Chlorocebus sabaeus) placenta and its relation to gestational age.

BACKGROUND: Focus on the placenta as an agent of fetal development and offspring health outcomes is growing. Primate research facilities or zoos may collect and fix placental tissue for long-term storage, but little is known about the effects of formalin fixation on the non-human primate placenta. METHODS: We obtained 48 vervet monkey placentas from the St. Kitts Biomedical Research Foundation. We investigated via correlation coefficients and ANOVAs the effects of gestational age and original fresh weight on weight change due to fixation. We also used linear regression models to determine whether fixed tissue weight was predictive of fresh weight and gestational age. RESULTS: Although the vervet monkey placenta is described as bidiscoid, 14.6% of the placentas in this sample were fused into a single mass. A decrease in weight was the most common response to formalin fixation, with the greatest degree of loss experienced by the heaviest placentas (ANOVA, F=5.99, P=0.005). Gestational age was unrelated to weight change. Those placentas that increased in weight had the lowest fresh weights. Fixed weights significantly predicted both fresh weight and gestational age (r(2) =0.78, P<0.00001; r(2) =0.76, P<0.00001, respectively). CONCLUSIONS: This paper adds to a sparse literature on the vervet monkey placenta. That fixed placentas are excellent predictors of both fresh weight and gestational age suggests that banked tissue may be a valuable resource for reconstructing aspects of individual life history, although caution must be exercised given the variability of weight change as a function of original placental size.

Possible thermoregulatory functions of the internal vertebral venous plexus in man and various other mammals: evidence from comparative anatomical studies.

Comparative anatomy was used to collect more evidence for a thermoregulatory function of the internal vertebral venous plexus (IVVP). The venous connections of the IVVP were studied and compared in various mammals in order to find evidence for the existence of climate related anatomical adaptations. Humans and vervet monkeys were chosen as representatives of mammals living in moderate climates, the IVVP of the dolphin was studied because this animal is always surrounded by cold water. The springbok was chosen as a representative of mammalian species living under very hot conditions. The present study was exclusively performed on post mortem material. After filling the venous system with latex the IVVP and its venous connections were dissected. It appeared that in the dolphin, veins from the trunk muscles were directly and exclusively connected to the IVVP in the absence of an azygos vein. In the vervet monkey and human specimens, veins originating in the muscles drained both into the caval veins and into the IVVP. In these mammals veins draining from brown fat areas were also connected to the IVVP. In the springbok, drainage of blood from the muscles was prevented to enter the IVVP by the presence of valves. In humans and vervet monkeys we found that the lumbar parts of the IVVP were connected to subcutaneous veins of the back. It was concluded that the anatomy of the IVVP and its connecting veins may serve to thermoregulate the spinal cord and that climate related anatomical adaptations were present in the species studied.

A web-based brain atlas of the vervet monkey, Chlorocebus aethiops.

Vervet monkeys are a frequently studied animal model in neuroscience research. Although equally distantly related to humans, the ancestors of vervets diverged from those of macaques and baboons more than 11 million years ago, antedating the divergence of the ancestors of humans, chimpanzees and gorillas. To facilitate anatomic localization in the vervet brain, two linked on-line electronic atlases are described, one based on registered MRI scans from hundreds of vervets (http://www.loni.ucla.edu/Research/Atlases/Data/vervet/vervetmratlas/vervetmratlas.html) and the other based on a high-resolution cryomacrotome study of a single vervet (http://www.loni.ucla.edu/Research/Atlases/Data/vervet/vervetatlas/vervetatlas.html). The averaged MRI atlas is also available as a volume in Neuroimaging Informatics Technology Initiative format. In the cryomacrotome atlas, various sulcal and subcortical structures have been anatomically labeled and surface rendered views are provided along the primary planes of section. Both atlases simultaneously provide views in all three primary planes of section, rapid navigation by clicking on the displayed images, and stereotaxic coordinates in the averaged MRI atlas space. Despite the extended time period since their divergence, the major sulcal and subcortical landmarks in vervets are highly conserved relative to those described in macaques.

The ultrastructure of the Sertoli cell of the vervet monkey, Chlorocebus aethiops.

The ultrastructure of the Sertoli cell of the vervet monkey was studied using both scanning and transmission electron microscopic techniques. SEM micrographs revealed perforated sleeve-like processes which encased mature elongated spermatids which are ready for spermiation. TEM micrographs showed a large Sertoli cell nucleus characterized by many lobes (4-5) and consisting of a homogenous nucleoplasm and a distinctive nucleolus. The nucleus occupies a significant portion of the basal region of the cell. The distribution of chromatin clearly shows high activity of these cells. Lipid droplets and free ribosomes are also found scattered throughout the cytoplasm. Well-developed Golgi apparatus is found in the basal region of the cell. There is phagocytic activity in the Sertoli cells as revealed by the presence of numerous phagosomes. Numerous mitochondria with well-developed tubular cristae are found on the basal side of the nucleus, whereas few mitochondria are located on the apical side of the nucleus. Distinct desmosomes are located between cells. A well-developed smooth endoplasmic reticulum and granular endoplasmic reticulum are frequently found in the cytoplasm of the Sertoli cells. The results of this investigation showed that Sertoli cells of the vervet monkey are almost similar to those of humans and show many similarities with other mammalian species.

Establishing a model spinal cord injury in the African green monkey for the preclinical evaluation of biodegradable polymer scaffolds seeded with human neural stem cells.

Given the involvement of post-mitotic neurons, long axonal tracts and incompletely elucidated injury and repair pathways, spinal cord injury (SCI) presents a particular challenge for the creation of preclinical models to robustly evaluate longitudinal changes in neuromotor function in the setting in the presence and absence of intervention. While rodent models exhibit high degrees of spontaneous recovery from SCI injury, animal care concerns preclude complete cord transections in non-human primates and other larger vertebrate models. To overcome such limitations a segmental thoracic (T9-T10) spinal cord hemisection was created and characterized in the African green monkey. Physiological tolerance of the model permitted behavioral analyses for a prolonged period post-injury, extending to predefined study termination points at which histological and immunohistochemical analyses were performed. Four monkeys were evaluated (one receiving no implant at the lesion site, one receiving a poly(lactide-co-glycolide) (PLGA) scaffold, and two receiving PLGA scaffolds seeded with human neural stem cells (hNSC)). All subjects exhibited Brown-Séquard syndrome 2 days post-injury consisting of ipsilateral hindlimb paralysis and contralateral hindlimb hypesthesia with preservation of bowel and bladder function. A 20-point observational behavioral scoring system allowed quantitative characterization of the levels of functional recovery. Histological endpoints including silver degenerative staining and Iba1 immunohistochemistry, for microglial and macrophage activation, were determined to reliably define lesion extent and correlate with neurobehavioral data, and justify invasive telemetered electromyographic and kinematic studies to more definitively address efficacy and mechanism.

Parafascicular nucleus projection to the extrastriatal basal ganglia in monkeys.

We have analyzed the parafascicular thalamic projection to extrastriatal structures of the basal ganglia using anterograde and retrograde tracing in monkeys. We identified (1) retrogradely labeled neurons in the parafascicular nucleus projecting to the anteromedial, limbic part of the external and internal pallidum, the substantia nigra and the subthalamic nucleus, (2) labeled terminals scattered in all these structures after anterograde tracer injection into the medial part of the parafascicular nucleus and (3) individual parafascicular terminals that arborized rather poorly in a large portion of each basal ganglia structure. Our study provides evidence that the parafascicular nucleus, and especially its medial part, can relay emotional and motivational information back to all basal ganglia components in primates.

Specializations of the granular prefrontal cortex of primates: implications for cognitive processing.

The biological underpinnings of human intelligence remain enigmatic. There remains the greatest confusion and controversy regarding mechanisms that enable humans to conceptualize, plan, and prioritize, and why they are set apart from other animals in their cognitive abilities. Here we demonstrate that the basic neuronal building block of the cerebral cortex, the pyramidal cell, is characterized by marked differences in structure among primate species. Moreover, comparison of the complexity of neuron structure with the size of the cortical area/region in which the cells are located revealed that trends in the granular prefrontal cortex (gPFC) were dramatically different to those in visual cortex. More specifically, pyramidal cells in the gPFC of humans had a disproportionately high number of spines. As neuron structure determines both its biophysical properties and connectivity, differences in the complexity in dendritic structure observed here endow neurons with different computational abilities. Furthermore, cortical circuits composed of neurons with distinguishable morphologies will likely be characterized by different functional capabilities. We propose that 1. circuitry in V1, V2, and gPFC within any given species differs in its functional capabilities and 2. there are dramatic differences in the functional capabilities of gPFC circuitry in different species, which are central to the different cognitive styles of primates. In particular, the highly branched, spinous neurons in the human gPFC may be a key component of human intelligence.