Observations on the anatomy of the funiculus spermaticus and the testis in Brachyteles sp. (SPIX, 1823) primates - Atelidae.

BACKGROUND: Analysing the literature about the reproductive anatomy on New World Primates, one can see the need of standardisation on the description methods and, more importantly, the lack of detailed information. The problem is aggravated by the difficult access to specimens of the endangered species such as Brachyteles sp. This paper's objective was to extend knowledge on the male reproductive anatomy of these primates. The testis and funiculus spermaticus of Brachyteles are described in detail. METHODS: We utilised one individual of Brachyteles arachnoides, two hybrids (B. arachnoides × Brachyteles hypoxanthus) and photographs of the testis of a third fresh specimen of a hybrid individual. RESULTS: The septum formed by tunica dartos adheres to the testis and separates the scrotum in two testicular cavities. Passed the spermatic cord, the external spermatic fascia continues with the tunica dartos, covering the cranial half of the testis. The fascia cremasterica divides itself in bundles of fibres and forms loops around the testicles creating a sac like structure that seems to be unique among Neotropical Primates. The appendix testis is described for the first time in platyrrhini. It is presented as a sessile structure in the extremitas capitata of the testis. Previous literature on the reproductive anatomy of platyrrhini is limited. Despite that, it can be said that the large size and volume of the testis, and complex structure of the cremaster, could consist of a heat loss reduction strategy in cold and humid forest environments. CONCLUSIONS: Except for the larger size of the testicles in hybrid individuals, no other significant morphological differences were found between B. arachnoides and hybrids (B. arachnoides × B. hypoxanthus).

Correlation between musculoskeletal structure of the hand and primate locomotion: Morphometric and mechanical analysis in prehension using the cross- and triple-ratios.

Biometric ratios of the relative length of the rays in the hand have been analyzed between primate species in the light of their hand function or phylogeny. However, how relative lengths among phalanges are mechanically linked to the grasping function of primates with different locomotor behaviors remains unclear. To clarify this, we calculated cross and triple-ratios, which are related to the torque distribution, and the torque generation mode at different joint angles using the lengths of the phalanges and metacarpal bones in 52 primates belonging to 25 species. The torque exerted on the finger joint and traction force of the flexor tendons necessary for a cylindrical grip and a suspensory hand posture were calculated using the moment arm of flexor tendons measured on magnetic resonance images, and were compared among Hylobates spp., Ateles sp., and Papio hamadryas. Finally, the torques calculated from the model were validated by a mechanical study detecting the force exerted on the phalanx by pulling the digital flexor muscles during suspension in these three species. Canonical discriminant analysis of cross and triple-ratios classified primates almost in accordance with their current classification based on locomotor behavior. The traction force was markedly reduced with flexion of the MCP joint parallel to the torque in brachiating primates; this was notably lower in the terrestrial quadrupedal primates than in the arboreal primates at mild flexion. Our mechanical study supported these features in the torque and traction force generation efficiencies. Our results suggest that suspensory or terrestrial quadrupedal primates have hand structures that can exert more torque at a suspensory posture, or palmigrade and digitigrade locomotion, respectively. Furthermore, our study suggests availability of the cross and triple-ratios as one of the indicators to estimate the hand function from the skeletal structure.

Trabecular architecture and joint loading of the proximal humerus in extant hominoids, Ateles, and Australopithecus africanus.

OBJECTIVES: Several studies have investigated potential functional signals in the trabecular structure of the primate proximal humerus but with varied success. Here, we apply for the first time a "whole-epiphyses" approach to analysing trabecular bone in the humeral head with the aim of providing a more holistic interpretation of trabecular variation in relation to habitual locomotor or manipulative behaviors in several extant primates and Australopithecus africanus. MATERIALS AND METHODS: We use a "whole-epiphysis" methodology in comparison to the traditional volume of interest (VOI) approach to investigate variation in trabecular structure and joint loading in the proximal humerus of extant hominoids, Ateles and A. africanus (StW 328). RESULTS: There are important differences in the quantification of trabecular parameters using a "whole-epiphysis" versus a VOI-based approach. Variation in trabecular structure across knuckle-walking African apes, suspensory taxa, and modern humans was generally consistent with predictions of load magnitude and inferred joint posture during habitual behaviors. Higher relative trabecular bone volume and more isotropic trabeculae in StW 328 suggest A. africanus may have still used its forelimbs for arboreal locomotion. DISCUSSION: A whole-epiphysis approach to analysing trabecular structure of the proximal humerus can help distinguish functional signals of joint loading across extant primates and can provide novel insight into habitual behaviors of fossil hominins.

Fetal development of the Poeppig's woolly monkey (Lagothrix poeppigii).

The intrauterine development is an evolutionary strategy that prepares the neonate for extra-uterine life, thus providing important information on the life history of species. In this study, we described the external and internal morphology of 25 fetuses of Poeppig's woolly monkeys (Lagothrix poeppigii) by taking advantage of a 10-year participatory collection of biological samples originated from animals hunted for subsistence purposes in the Peruvian Amazon. Logistic regressions estimated the probability of occurrence of each external morphological characteristic in relation to the crown-rump length (CRL). The presence of nails, closed eyelids, differentiated genitalia and formed limbs with separation of the digits were observed in all analyzed fetuses (≥4.2 cm CRL). The other characteristics appeared in the following order: skin with epidermal pigmentation, oral and nasal mucosal pigmentation, tactile pelage and covering pelage. Although advanced fetuses (>15.8 cm CRL) showed most fetal external characteristics, they were not fully developed and no specimen showed tooth eruption or opened eyelids. The growth formula used to determine fetal age was ∛W = 0.042 (t - 45), with a high linear relationship between CRL and gestational age. All associations between the external biometry, absolute volume of internal organs and the CRL had a high coefficient of determination. Advanced fetuses and adults showed similar relative volume of thoracic and abdominal organs, except for thymus and the liver with a higher and lower relative volume, respectively. The relative volume of the tubular gastrointestinal tract and the thymus had a constant increase along fetal development, and the liver showed a significant decrease. This study describes important morphological events for understanding the gestational development in the Lagothrix genus. In addition, these results may be useful to improve imaging techniques, contributing to the in situ and ex situ reproductive management of this highly hunted species in the Amazon.

Determination of vertebral heart score in three species of Spider monkey (Ateles fusciceps, A. hybridus and A. paniscus).

BACKGROUND: The vertebral heart score (VHS) is a method of evaluation of cardiac size well documented in domestic mammals and in other primate species, and the aim of this study was to determine the VHS in three species of Spider monkey. METHODS: In this retrospective study, right lateral radiographs of thirty clinically well animals were reviewed and VHS determined. The species included were Ateles fusciceps (n=17), Ateles hybridus (n=8) and Ateles paniscus (n=5). RESULTS: The VHS was found to vary between species and was 9.73±0.81 for A. fusciceps, 10.53±0.37 for A. hybridus and 10.45±0.27 for A. paniscus. CONCLUSIONS: The observed values appear consistent with values determined for other primate species. There was statistically significant variation noted between species, and so VHS should be considered species-specific in this genus. The values determined may be of benefit in objectively evaluating cardiac size in the species investigated.

Membrane-plate transition in leaves as an influence on dietary selectivity and tooth form.

Primates need accurate sensory signals about food quality to forage efficiently. Current evidence suggests that they target leaf foods based on color at long-range, reinforcing this with post-ingestive sensations relating to leaf toughness evoked during chewing. Selection against tough leaves effectively selects against high fiber content, which in turn gives a greater opportunity of acquiring protein. Here we consider a novel intermediate mechanical factor that could aid a folivore: leaves may transform mechanically from membranes (sheets that cannot maintain their shape under gravitational loads and thus 'flop') early on in development into plates (that can maintain their shape) as they mature. This transformation can be detected visually. Mechanical tests on two species of leaf eaten by southern muriqui monkeys (Brachyteles arachnoides) in Southern Atlantic Forest, Brazil, support a membrane-to-plate shift in turgid leaves during their development. A measure of this mechanical transition, termed lambda (λ), was found to correlate with both leaf color and toughness, thus supporting a potential role in leaf selection. Muriquis appear to select membranous leaves, but they also eat leaves that are plate-like. We attribute this to the degree of cresting of their molar teeth. A dietary choice restricted to membranous leaves might typify the type of 'fallback' leaf that even frugivorous primates will target because membranes of low toughness are relatively easily chewed. This may be relevant to the diets of hominins because these lack the bladed postcanine teeth seen in mammals with a specialized folivorous diet. We suggest that mammals with such dental adaptations can consume tougher leaf 'plates' than others.

Anatomicohistological characteristics of the tubular genital organs of the female woolly monkey (Lagothrix poeppigii).

Functional morphology of the reproductive organs is a key component for the better understanding of reproductive patterns as well to maximize reproductive efficiency and to develop assisted breeding techniques adapted to wildlife. This study examined anatomical and histological characteristics of genital organs of 60 Poeppig's woolly monkey females in the wild in different reproductive stages, collected by rural hunters in the northeastern Peruvian Amazon. The endometrium, the endometrial glands, and the myometrium showed a significant increase in size related to the follicular growth. In nonpregnant females in the follicular phase, the endometrium, the endometrial glands, and the myometrium showed a significant increase related to the follicular growth. Nonpregnant females in the luteal phase had a thicker endometrium, a greater proliferation of endometrial glands, and a thicker myometrium, compared to females in the follicular phase. Nonpregnant females with small antral follicles presented high amounts of collagen beneath the endometrial epithelium, a sign of endometrial regeneration after menstruation that could be useful for the diagnosis of the reproductive phase in this species. A larger proportion of secreting cervical glands was observed in pregnant females compared to other females. The cervical mucous secretion occupied the lumen of the endocervical canal, assuring that no material could enter the uterus during gestation. The Poeppig's woolly monkey showed different vaginal epithelium features in accordance with the reproductive state of the female, suggesting that vaginal cytology could be a successful methodology with which to characterize the estrous cycle of wild primates. The present reproductive evaluation of Poeppig's woolly monkey provides important information that could improve the methodologies for the diagnosis of the reproductive phase of females, the assisted reproductive techniques in non-human primates, and could also give us opportunity for comparative studies and an insight into the evolution of animal reproductive biology, including humans.

Mechanoreceptivity of prehensile tail skin varies between ateline and cebine primates.

Prehensile tails evolved independently twice in primates: once in the ateline subfamily of platyrrhine primates and once in the genus Cebus. Structurally, the prehensile tails of atelines and Cebus share morphological features distinguishing them from nonprehensile tails (e.g., robust and strong caudal vertebrae, well developed lateral tail musculature, etc.). However, because of their independent evolutionary histories, the prehensile tails of atelines exhibit some differences from the Cebus prehensile tail. Ateline tails are relatively longer than those of Cebus, and they have less well-developed extensor compartment musculature. However, perhaps the most obvious difference is the distinctive hairless friction pad on the ventrodistal surface of the ateline tail; the tail of Cebus is completely covered in hair. This study documents the presence of four epicritic histologic mechanoreceptors in the friction pad of atelines: Meissner's corpuscles, Pacinian corpuscles, Ruffini corpuscles, and Merkel discs. Ruffini corpuscles and Merkel cells were also identified in the ventrodistal skin of the Cebus tail. However, Meissner's and Pacinian corpuscles (not typically associated with hairy skin) were not found in Cebus. Cebus was also compared to its closest living sister taxon, nonprehensile-tailed Saimiri, in which genus only Ruffini corpuscles are observed (no Merkel discs). The differences in mechanoreceptor type and morphology are attributed to the contrasting behavioral and tactile demands of the tail as it is used in posture and locomotion, which also distinguishes atelines from Cebus.

The evolution of brachiation in ateline primates, ancestral character states and history.

This study examines how brachiation locomotion evolved in ateline primates using recently-developed molecular phylogenies and character reconstruction algorithms, and a newly-collected dataset including the fossils Protopithecus, Caipora, and Cebupithecia. Fossils are added to two platyrrhine molecular phylogenies to create several phylogenetic scenarios. A generalized least squares algorithm reconstructs ateline and atelin ancestral character states for 17 characters that differentiate between ateline brachiators and nonbrachiators. Histories of these characters are mapped out on these phylogenies, producing two scenarios of ateline brachiation evolution that have four commonalities: First, many characters change towards the Ateles condition on the ateline stem lineage before Alouatta splits off from the atelins, suggesting that an ateline energy-maximizing strategy began before the atelines diversified. Second, the ateline last common ancestor is always reconstructed as an agile quadruped, usually with suspensory abilities. It is never exactly like Alouatta and many characters reverse and change towards the Alouatta condition after Alouatta separates from the atelins. Third, most characters undergo homoplastic change in all ateline lineages, especially on the Ateles and Brachyteles terminal branches. Fourth, ateline character evolution probably went through a hindlimb suspension with tail-bracing phase. The atelines most likely diversified via a quick adaptive radiation, with bursts of punctuated change occurring in their postcranial skeletons, due to changing climatic conditions, which may have caused competition among the atelines and between atelines and pitheciines.

Taxon combinations, parsimony analysis (PAUP*), and the taxonomy of the yellow-tailed woolly monkey, Lagothrix flavicauda.

The classifications of primates, in general, and platyrrhine primates, in particular, have been greatly revised subsequent to the rationale for taxonomic decisions shifting from one rooted in the biological species concept to one rooted solely in phylogenetic affiliations. Given the phylogenetic justification provided for revised taxonomies, the scientific validity of taxonomic distinctions can be rightly judged by the robusticity of the phylogenetic results supporting them. In this study, we empirically investigated taxonomic-sampling effects on a cladogram previously inferred from craniodental data for the woolly monkeys (Lagothrix). We conducted the study primarily through much greater sampling of species-level taxa (OTUs) after improving some character codings and under a variety of outgroup choices. The results indicate that alternative selections of species subsets from within genera produce various tree topologies. These results stand even after adjusting the character set and considering the potential role of interobserver disagreement. We conclude that specific taxon combinations, in this case, generic or species pairings, of the primary study group has a biasing effect in parsimony analysis, and that the cladistic rationale for resurrecting the Oreonax generic distinction for the yellow-tailed woolly monkey (Lagothrix flavicauda) is based on an artifact of idiosyncratic sampling within the study group below the genus level. Some recommendations to minimize the problem, which is prevalent in all cladistic analyses, are proposed.

Knuckle walking signal in the manual digits of Pan and Gorilla.

This article examines the curvature of the manual proximal and middle phalanges of species belonging to Pan, Gorilla, Ateles, Macaca, Pongo, Hylobates, and Cebus to determine whether middle phalangeal curvature, when considered in conjunction with proximal phalangeal curvature, yields a locomotor signal. Prior studies have demonstrated the discriminatory power of proximal phalanges for separating suspensory species (including knuckle walkers) from pronograde quadrupedal species, but less emphasis has been placed on the distinguishing phalangeal characteristics of taxa within the suspensory category. This study demonstrates, first, that middle phalanges discriminate suspensory from nonsuspensory species, although not as cleanly as proximal phalanges. Finer discrimination of locomotor signals, including subtle differences among animals employing different modes of suspension, is possible through a comparison of the curvatures of the proximal phalanges and corresponding middle phalanges. Their relative curvature differs in quadrupeds, brachiators, and knuckle walkers. Knuckle walkers (Pan and Gorilla) have relatively little curvature of the middle phalanges coupled with marked curvature of the proximal phalanges, whereas brachiators (Ateles and Hylobates) display marked curvature of both proximal and middle phalanges, and pronograde quadrupeds (Cebus and Macaca) have relatively straight proximal and moderately curved middle phalanges. Quadrumanous climbers (Pongo) have a unique combination of traits, whereby curvature is high in both proximal and middle phalanges, but less so in the latter than the former. These differences, predictable on the basis of the biomechanical forces to which digits are subjected, may open a new venue for future research on the locomotor repertoire of prebipedal ancestors of hominins.

Nonhuman anthropoid primate femoral neck trabecular architecture and its relationship to locomotor mode.

Functional analyses of human and nonhuman anthropoid primate femoral neck structure have largely ignored the trabecular bone. We tested hypotheses regarding differences in the relative distribution and structural anisotropy of trabecular bone in the femoral neck of quadrupedal and climbing/suspensory anthropoids. We used high-resolution X-ray computed tomography to analyze quantitatively the femoral neck trabecular structure of Ateles geoffroyi, Symphalangus syndactylus, Alouatta seniculus, Colobus guereza, Macaca fascicularis, and Papio cynocephalus (n = 46). We analyzed a size-scaled superior and inferior volume of interest (VOI) in the femoral neck. The ratio of the superior to inferior VOI bone volume fraction indicated that the distribution of trabecular bone was inferiorly skewed in most (but not all) quadrupeds and evenly distributed the climbing/suspensory species, but interspecific comparisons indicated that all taxa overlapped in these measurements. Degree of anisotropy values were generally higher in the inferior VOI of all species and the results for the two climbing/suspensory taxa, A. geoffroyi (1.71 +/- 0.30) and S. syndactylus (1.55 +/- 0.04), were similar to the results for the quadrupedal anthropoids, C. guereza (male = 1.64 +/- 0.13; female = 1.68 +/- 0.07) and P. cynocephalus (1.47 +/- 0.13). These results suggest strong trabecular architecture similarity across body sizes, anthropoid phylogenetic backgrounds, and locomotor mode. This structural similarity might be explained by greater similarity in anthropoid hip joint loading mechanics than previously considered. It is likely that our current models of anthropoid hip joint mechanics are overly simplistic.

Functional morphology of the first cervical vertebra in humans and nonhuman primates.

The cervical vertebral column bears or balances the weight of the head supported by the nuchal muscles that partly originate from the cervical vertebrae. The position of the head relative to the vertebral column, and consequently locomotion and posture behavior, could thus be associated with the form of the cervical vertebrae. In spite of this assumption and some empirical indications along these lines, primate vertebral morphologies have been reported to be very similar and not clearly related to locomotion. We therefore study the relationship between the morphology of the first cervical vertebra, the atlas, and the locomotion pattern within primates using a geometric morphometric approach. Our analysis is based on a total of 116 vertebrae of adult Homo sapiens, Gorilla gorilla, Pan troglodytes, Pongo pygmaeus, Hylobates lar, Macaca mulatta, Papio hamadryas, Ateles geoffroyi, and Alouatta palliata. On each atlas, 56 landmarks were digitized and superimposed by Procrustes registration. The resulting shape variables were analyzed by principal component analysis, multivariate regression, and partial least-squares analysis. We found that the nine primate species differ clearly in their atlas morphology and that allometric shape change is distinct between the nonhuman primates and Homo sapiens. We could further identify morphological features that relate to the species' locomotion pattern. Human atlas shape, however, cannot be predicted by an extrapolation of the nonhuman primate model. This implies that either the primate atlas is generalized enough to allow bipedal locomotion or else the human atlas morphology is a unique adaptation different from that in the more orthograde nonhuman primates.