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Showing papers on "Primate published in 2013"


Journal ArticleDOI
TL;DR: It is shown that rhesus monkeys can control their vocalizations in a goal-directed way, suggesting a cardinal role of the monkey homologue of Broca's area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.
Abstract: Broca's area in the ventrolateral prefrontal cortex (vlPFC) has a crucial role in human volitional speech production; damage to this area causes severe impairment of speech production. Lesions in PFC of monkeys, however, have only mild effects on spontaneous vocal behaviour. Non-human primate vocalizations are thus believed to constitute affective utterances processed by a subcortical network. Here in contrast to this assumption, we show that rhesus monkeys can control their vocalizations in a goal-directed way. During single-cell recordings in the vlPFC of monkeys trained to vocalize in response to visual cues, we find call-related neurons that specifically predict the preparation of instructed vocalizations. The activity of many call-related neurons before vocal output correlates with call parameters of instructed vocalizations. These findings suggest a cardinal role of the monkey homologue of Broca's area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.

117 citations


Journal ArticleDOI
TL;DR: This work analyzed the complete mitochondrial cytochrome b gene of 126 samples using feces from wild individuals and material from zoo and museum specimens with clear geographical provenance, implying that the mtDNA diversity of African green monkeys does not conform to existing taxonomic classifications.
Abstract: African green monkeys (Chlorocebus) represent a widely distributed and morphologically diverse primate genus in sub-Saharan Africa. Little attention has been paid to their genetic diversity and phylogeny. Based on morphological data, six species are currently recognized, but their taxonomy remains disputed. Here, we aim to characterize the mitochondrial (mt) DNA diversity, biogeography and phylogeny of African green monkeys. We analyzed the complete mitochondrial cytochrome b gene of 126 samples using feces from wild individuals and material from zoo and museum specimens with clear geographical provenance, including several type specimens. We found evidence for nine major mtDNA clades that reflect geographic distributions rather than taxa, implying that the mtDNA diversity of African green monkeys does not conform to existing taxonomic classifications. Phylogenetic relationships among clades could not be resolved suggesting a rapid early divergence of lineages. Several discordances between mtDNA and phenotype indicate that hybridization may have occurred in contact zones among species, including the threatened Bale monkey (Chlorocebus djamdjamensis). Our results provide both valuable data on African green monkeys’ genetic diversity and evolution and a basis for further molecular studies on this genus. Am. J. Primatol. 75:350-360, 2013. © 2013 Wiley Periodicals, Inc.

91 citations


Journal ArticleDOI
TL;DR: The results are compatible with a homologous organization of the prefrontal cortex in New and Old World monkeys, and suggest significant parallels between the present pathways, revealed by tract-tracing, and networks revealed by functional connectivity analysis in Old World monkey and humans.
Abstract: Contemporary studies recognize 3 distinct cytoarchitectural and functional areas within the Brodmann area 8 complex, in the caudal prefrontal cortex: 8b, 8aD, and 8aV. Here, we report on the quantitative characteristics of the cortical projections to these areas, using injections of fluorescent tracers in marmoset monkeys. Area 8b was distinct from both 8aD and 8aV due to its connections with medial prefrontal, anterior cingulate, superior temporal polysensory, and ventral midline/retrosplenial areas. In contrast, areas 8aD and 8aV received the bulk of the projections from posterior parietal cortex and dorsal midline areas. In the frontal lobe, area 8aV received projections primarily from ventrolateral areas, while both 8aD and 8b received dense inputs from areas on the dorsolateral surface. Whereas area 8aD received the most significant auditory projections, these were relatively sparse, in comparison with those previously reported in macaques. Finally, area 8aV was distinct from both 8aD and 8b by virtue of its widespread input from the extrastriate visual areas. These results are compatible with a homologous organization of the prefrontal cortex in New and Old World monkeys, and suggest significant parallels between the present pathways, revealed by tract-tracing, and networks revealed by functional connectivity analysis in Old World monkeys and humans.

86 citations


Journal ArticleDOI
TL;DR: Investigating personality structure in the brown capuchin monkey, a New World primate species, and comparing this structure to those of chimpanzees, orangutans, and rhesus macaques reveals that brown capuchins and great apes overlapped in personality structure, particularly chimpanzees in the case of Neuroticism.
Abstract: Species comparisons of personality structure (i.e. how many personality dimensions and the characteristics of those dimensions) can facilitate questions about the adaptive function of personality in nonhuman primates. Here we investigate personality structure in the brown capuchin monkey (Sapajus apella), a New World primate species, and compare this structure to those of chimpanzees (Pan troglodytes), orangutans (Pongo spp.), and rhesus macaques (Macaca mulatta). Brown capuchins evolved behavioral and cognitive traits that are qualitatively similar to those of great apes, and individual differences in behavior and cognition are closely associated with differences in personality. Thus, we hypothesized that brown capuchin personality structure would overlap more with great apes than with rhesus macaques. We obtained personality ratings from seven sites on 127 brown capuchin monkeys. Principal-components analysis identified five personality dimensions (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness), which were reliable across raters and, in a subset of subjects, significantly correlated with relevant behaviors up to a year later. Comparisons between species revealed that brown capuchins and great apes overlapped in personality structure, particularly chimpanzees in the case of Neuroticism. However, in some respects (i.e. capuchin Sociability and Openness) the similarities between capuchins and great apes were not significantly greater than those between capuchins and rhesus macaques. We discuss the relevance of our results to brown capuchin behavior, and the evolution of personality structure in primates.

82 citations


Journal ArticleDOI
TL;DR: It is shown that squirrel monkeys (Saimiri sciureus) can detect abstract, non-adjacent dependencies in auditory stimuli, and this constitutes the first pattern learning study where artificial stimuli were designed with the species' communication system in mind.
Abstract: Sensitivity to dependencies (correspondences between distant items) in sensory stimuli plays a crucial role in human music and language. Here, we show that squirrel monkeys (Saimiri sciureus) can detect abstract, non-adjacent dependencies in auditory stimuli. Monkeys discriminated between tone sequences containing a dependency and those lacking it, and generalized to previously unheard pitch classes and novel dependency distances. This constitutes the first pattern learning study where artificial stimuli were designed with the species' communication system in mind. These results suggest that the ability to recognize dependencies represents a capability that had already evolved in humans’ last common ancestor with squirrel monkeys, and perhaps before.

53 citations


Journal ArticleDOI
TL;DR: The data provide perceptual evidence for the theory that speech may have evolved from ancestral primate rhythmic facial expressions by lending behavioral support for the hypothesis that perceptual processes in monkeys are similarly tuned to the natural frequencies of communication signals as they are in humans.
Abstract: Human speech universally exhibits a 3- to 8-Hz rhythm, corresponding to the rate of syllable production, which is reflected in both the sound envelope and the visual mouth movements. Artificial perturbation of the speech rhythm outside the natural range reduces speech intelligibility, demonstrating a perceptual tuning to this frequency band. One theory posits that the mouth movements at the core of this speech rhythm evolved through modification of ancestral primate facial expressions. Recent evidence shows that one such communicative gesture in macaque monkeys, lip-smacking, has motor parallels with speech in its rhythmicity, its developmental trajectory, and the coordination of vocal tract structures. Whether monkeys also exhibit a perceptual tuning to the natural rhythms of lip-smacking is unknown. To investigate this, we tested rhesus monkeys in a preferential-looking procedure, measuring the time spent looking at each of two side-by-side computer-generated monkey avatars lip-smacking at natural versus sped-up or slowed-down rhythms. Monkeys showed an overall preference for the natural rhythm compared with the perturbed rhythms. This lends behavioral support for the hypothesis that perceptual processes in monkeys are similarly tuned to the natural frequencies of communication signals as they are in humans. Our data provide perceptual evidence for the theory that speech may have evolved from ancestral primate rhythmic facial expressions.

52 citations


Journal ArticleDOI
TL;DR: From millions of retroposons, the authors found 104 perfect orthologous insertions in both tarsiers and anthropoids to the exclusion of strepsirrhines, providing conflict-free evidence for the Haplorrhini hypothesis, and none supporting either of the other two positions.
Abstract: One of the most disputed issues in primate evolution and thus of our own primate roots, is the phylogenetic position of the Southeast Asian tarsier. While much molecular data indicate a basal place in the primate tree shared with strepsirrhines (prosimian monophyly hypothesis), data also exist supporting either an earlier divergence in primates (tarsier-first hypothesis) or a close relationship with anthropoid primates (Haplorrhini hypothesis). The use of retroposon insertions embedded in the Tarsius genome afforded us the unique opportunity to directly test all three hypotheses via three pairwise genome alignments. From millions of retroposons, we found 104 perfect orthologous insertions in both tarsiers and anthropoids to the exclusion of strepsirrhines, providing conflict-free evidence for the Haplorrhini hypothesis, and none supporting either of the other two positions. Thus, tarsiers are clearly the sister group to anthropoids in the clade Haplorrhini.

51 citations


Journal ArticleDOI
TL;DR: It is suggested that colobus monkeys eating diets with differing amounts of species and parts may ultimately receive similar concentrations of nutrients.
Abstract: Within a primate species, diet can be highly variable in composition, even at small spatial scales within the same forest, or temporally, suggesting that primates use different plant species and parts to meet similar nutritional needs. To test whether such differences in the plant species and parts that primates eat affects the nutrient concentrations that they obtain, we observed feeding of seven groups of red colobus monkeys (Procolobus rufomitratus) residing in Kibale National Park, Uganda. The different groups consumed mostly young leaves from many of the same plant species, but spent different amounts of time feeding on them. As protein and fibre are suggested to be important determinants of colobine food choice and abundance, we analysed multiple samples of 47 food species for protein and fibre. Despite the differences in the plant species and parts eaten, the protein and fibre concentrations for the seven red colobus groups were similar. Our results suggest that colobus monkeys eating diets with differing amounts of species and parts may ultimately receive similar concentrations of nutrients.

26 citations


Journal ArticleDOI
12 Feb 2013-PeerJ
TL;DR: It is proposed that the squirrel monkeys’ learning, observed in the experimental open diffusion tests, can be best described by a combination of social learning mechanisms in concert; in this case, those mechanisms are most likely object movement reenactment and social facilitation.
Abstract: Although the social learning abilities of monkeys have been well documented, this research has only focused on a few species. Furthermore, of those that also incorporated dissections of social learning mechanisms, the majority studied either capuchins (Cebus apella) or marmosets (Callithrix jacchus). To gain a broader understanding of how monkeys gain new skills, we tested squirrel monkeys (Saimiri boliviensis) which have never been studied in tests of social learning mechanisms. To determine whether S. boliviensis can socially learn, we ran "open diffusion" tests with monkeys housed in two social groups (N = 23). Over the course of 10 20-min sessions, the monkeys in each group observed a trained group member retrieving a mealworm from a bidirectional task (the "Slide-box"). Two thirds (67%) of these monkeys both learned how to operate the Slide-box and they also moved the door significantly more times in the direction modeled by the trained demonstrator than the alternative direction. To tease apart the underlying social learning mechanisms we ran a series of three control conditions with 35 squirrel monkeys that had no previous experience with the Slide-box. The first replicated the experimental open diffusion sessions but without the inclusion of a trained model, the second was a no-information control with dyads of monkeys, and the third was a 'ghost' display shown to individual monkeys. The first two controls tested for the importance of social support (mere presence effect) and the ghost display showed the affordances of the task to the monkeys. The monkeys showed a certain level of success in the group control (54% of subjects solved the task on one or more occasions) and paired controls (28% were successful) but none were successful in the ghost control. We propose that the squirrel monkeys' learning, observed in the experimental open diffusion tests, can be best described by a combination of social learning mechanisms in concert; in this case, those mechanisms are most likely object movement reenactment and social facilitation. We discuss the interplay of these mechanisms and how they related to learning shown by other primate species.

24 citations


Journal ArticleDOI
TL;DR: It is suggested that interspecies transmission of NHP beta- and gammaherpesviruses is, at most, a rare event in the wild.
Abstract: Emergence of viruses into the human population by transmission from nonhuman primates (NHPs) represents a serious potential threat to human health that is primarily associated with the increased bushmeat trade. Transmission of RNA viruses across primate species appears to be relatively frequent. In contrast, DNA viruses appear to be largely host specific, suggesting low transmission potential. Herein, we use a primate predator-prey system to study the risk of herpesvirus transmission between different primate species in the wild. The system was comprised of western chimpanzees (Pan troglodytes verus) and their primary (western red colobus, Piliocolobus badius badius) and secondary (black-and-white colobus, Colobus polykomos) prey monkey species. NHP species were frequently observed to be coinfected with multiple beta- and gammaherpesviruses (including new cytomegalo- and rhadinoviruses). However, despite frequent exposure of chimpanzees to blood, organs, and bones of their herpesvirus-infected monkey prey, there was no evidence for cross-species herpesvirus transmission. These findings suggest that interspecies transmission of NHP beta- and gammaherpesviruses is, at most, a rare event in the wild.

24 citations


Journal ArticleDOI
TL;DR: It is concluded that despite a long history of human disturbance on this landscape, spider monkeys were until recently successful at maintaining gene flow, and the recent decline is considered to be further indication of accelerated anthropogenic disturbance, but also of an opportunity to conserve native biodiversity.
Abstract: Spider monkeys (Genus: Ateles) are a widespread Neotropical primate with a highly plastic socioecological strategy. However, the Central American species, Ateles geoffroyi, was recently re-listed as endangered due to the accelerated loss of forest across the subcontinent. There is inconsistent evidence that spider monkey populations could persist when actively protected, but their long-term viability in unprotected, human-dominated landscapes is not known. We analyzed noninvasive genetic samples from 185 individuals in 14 putative social groups on the Rivas Isthmus in southwestern Nicaragua. We found evidence of weak but significant genetic structure in the mitochondrial control region and in eight nuclear microsatellite loci plus negative spatial autocorrelation in Fst and kinship. The overall pattern suggests strong localized mating and at least historical female-biased dispersal, as is expected for this species. Heterozygosity was significantly lower than expected under random mating and lower than that found in other spider monkey populations, possibly reflecting a recent decline in genetic diversity and a threat from inbreeding. We conclude that despite a long history of human disturbance on this landscape, spider monkeys were until recently successful at maintaining gene flow. We consider the recent decline to be further indication of accelerated anthropogenic disturbance, but also of an opportunity to conserve native biodiversity. Spider monkeys are one of many wildlife species in Central America that is threatened by land cover change, and an apt example of how landscape-scale conservation planning could be used to ensure long-term persistence.

Journal ArticleDOI
TL;DR: Although a systematic preference for soft white noise was found, Campbell's monkeys showed no preference for either consonant or dissonant sounds, which would suggest that human preference for consonant sounds is not systematically shared with New and Old World monkeys.
Abstract: The central position and universality of music in human societies raises the question of its phylogenetic origin. One of the most important properties of music involves harmonic musical intervals, in response to which humans show a spontaneous preference for consonant over dissonant sounds starting from early human infancy. Comparative studies conducted with organisms at different levels of the primate lineage are needed to understand the evolutionary scenario under which this phenomenon emerged. Although previous research found no preference for consonance in a New World monkey species, the question remained opened for Old World monkeys. We used an experimental paradigm based on a sensory reinforcement procedure to test auditory preferences for consonant sounds in Campbell's monkeys (Cercopithecus campbelli campbelli), an Old World monkey species. Although a systematic preference for soft (70 dB) over loud (90 dB) control white noise was found, Campbell's monkeys showed no preference for either consonant or dissonant sounds. The preference for soft white noise validates our noninvasive experimental paradigm, which can be easily reused in any captive facility to test for auditory preferences. This would suggest that human preference for consonant sounds is not systematically shared with New and Old World monkeys. The sensitivity for harmonic musical intervals emerged probably very late in the primate lineage.

Journal ArticleDOI
TL;DR: The behavioural strategies as well as the 3D kinematics of the whole forelimb and the trunk during the prehension of small static food items in five primate species in unconstrained conditions provide a good basis to suggest hypotheses concerning the factors involved in driving the evolution of grasping abilities in primates.

Journal ArticleDOI
TL;DR: This article used line transects to estimate population densities for four primate species in a mixed agroforest landscape up to a distance of 4000m from a forest reserve, in a region where no primate hunting takes place.

Journal Article
TL;DR: It is demonstrated that hair-pulling plays only a small role in alopecia in rhesus macaques, and at facilities reporting a sex-associated difference, more female macaques were reported to exhibit alopECia than were males.
Abstract: Alopecia (hair loss) is a substantial problem in rhesus macaque colonies, with an estimated prevalence of around 48% of animals exhibiting it at some point in their history12 and with numbers reaching as high as 68% in some populations.20 Hair loss can range from small focal areas to whole body parts (for example, the back) to the entire body missing hair.9,11,19 Although alopecia is not an uncommon condition, its etiology is not fully understood, with many contributing factors including seasonal variation, aging, rank, sex, housing condition, reproductive state, skin disorders, and nutritional deficiencies, behavioral pathology, and stress.5,12,17,20,22 Little is known about the relative contribution of various factors to alopecia in colony primates, but the assumption has often been that alopecia is primarily the result of a particular behavioral pathology (that is, hair-pulling) or the stress of the captive environment. Whatever the cause, alopecia is often considered to be a sign of poor welfare and subjected to increased regulatory attention.1,13 Hair-pulling is a syndrome that includes plucking hair from the body by using hands or teeth, manipulating it, and frequently ingesting it.3,14,17,18 Methods of hair removal range from pulling out fistfuls of hair to plucking out single hairs at a time to overgrooming (self-grooming in excess), and the resulting coat can have bald or patchy patterns.8 In cases where excessive hair is ingested by monkeys, gastric trichobezoars (that is, hair balls) can result, potentially leading to serious clinical complications.16 The prevalence of hair-pulling in individually housed monkeys is about 14% and is associated with increased age,14 but a more recent study reported overall rates as high as 33%.13 This pattern of hair-pulling is similar to that observed in the human disorder trichotillomania which also involves plucking out, and sometimes ingesting, hair.6,23 People have reported that hair-pulling is sometimes associated with increasing tension or stress, which can be alleviated with the act of pulling out hair.6,21 However, in rhesus macaques, stress does not appear to be a factor in hair loss.12,13 The true relationship between hair-pulling and alopecia is currently unknown. Although it is likely that hair-pulling produces hair loss in some rhesus macaques, it is unlikely that all cases of hair loss are attributable to the hair-pulling syndrome. In one study, a significantly higher proportion of rhesus monkeys with alopecia were observed to hair pull (53.9%), but 12.8% of the control population (with less than 10% hair loss) were observed to hair-pull, and for animals with alopecia, the location of the hair-pulling was not always near the site of alopecia.13 In addition, one singly housed rhesus monkey developed gastric trichobezoars from hair eating but was reported to have a good coat of hair.16 Further complicating this relationship between hair-pulling and alopecia is social housing. Monkeys can pull their own hair or that of others (or both). In a study of 2 breeding groups of rhesus macaques, monkeys pulled hair at the rate of 2.4 episodes per hour, and most of the episodes were directed toward other monkeys rather than to self (97% compared with 3%, respectively).18 In addition, limited enclosure space appears to have an additional effect on hair loss in group-housed rhesus monkeys.5,19 The purpose of the current study was to examine the relationship between alopecia and hair-pulling behavior in individually housed rhesus macaques in 4 primate colonies across the United States. There were 3 objectives. The first objective was to characterize the prevalence of alopecia and hair-pulling by using a simple ‘yes–no’ scoring system, with any hair loss or observation of hair-pulling scored as ‘yes.’ In the second objective, we examined prevalence as a function of facility. Animal management practices vary quite widely across primate facilities2 and may differentially affect the extent of both alopecia and hair-pulling. Therefore, we assessed commonalities and differences in alopecia and hair-pulling across primate centers. The final objective was to determine whether hair-pulling was a primary factor of hair loss in individually housed monkeys.

Book ChapterDOI
01 Jan 2013
TL;DR: Living hominoids (apes and humans), like Old World monkeys, are catarrhine primates, characterized by many specializations of how the postcranial skeleton relates to suspensory behavior.
Abstract: Living hominoids (apes and humans), like Old World monkeys, are catarrhine primates. Living apes are characterized by many specializations of how the postcranial skeleton relates to suspensory behavior. All are forest dwellers.They are divided into two families. The hylobatids, or lesser apes, are the gibbons and siamangs of Asia. They are frugivorous and folivorous and travel by brachiation, or arm swinging. They generally live in small monogamous groups. Hominids are the great apes and humans. The Asian orangutana are primarily frugivorous, mostly arboreal, and very suspensory. Adults are solitary foragers. The African great apes, gorillas, chimpanzees, and bonobos are found both in the trees and on the ground where they move by knuckle-walking. Gorillas are largely folivorous while chimps and bonobos are more frugivorous. All live in large groups, but have different social structures. Humans are very unusual primates and are found on all continents except Antarctica. We have very large brains, small teeth and reduced body hair. We have hands with a relatively long thumb and great manipulative abilities enabling extensive use of tools of many sorts. Our legs are relatively long and our feet have short toes with an adducted hallux. These features enable our bipedal locomotion, both walking and running. Human diets are very diverse and differ from those of other primates in that human food is often prepared by cooking. Humans live in a wide range of social structures, but all are characterized by extensive prosocial behavior with many adults involved in the raising of offspring. We have the slowest maturation and the longest lifespans of any primate, including long postreprodutive lives among human females.

Journal ArticleDOI
TL;DR: 130 high resolution electron micrographs from aging rhesus monkey (Macaca mulatta), provided by Alan Peters and his colleague, Claire Folger, represent 20 years of detailed study and are a valuable instrument to help gain better insight into the effects of normal aging on the neurons and neuroglial cells in the cerebral hemispheres and associated fiber tracts of the forebrain.
Abstract: In the spirit of sharing knowledge we decided to provide the means by which these images can be downloaded for educational purposes. The images are grouped into chapters, and users can download the images from each chapter (at a resolution of 6×9” at 240 dpi), but in addition, we have provided a download page so that users can obtain even higher resolution images (most of them 6×7” at 600 dpi) free of labeling and text. All images are available from our website, http://www.bu.edu/agingbrain. We have not included images of the structural appearance of components of cells and their processes in young monkeys, as such images can be found in the illustrations in the book, “The Fine Structure of the Nervous System: Neurons and Their Supporting Cells” 1991, by Alan Peters, Sanford L. Palay, and Henry deF. Webster, 3rd Edition, Oxford University Press. The reason for choosing to study the effects of normal aging in rhesus monkeys is that these primates provide a good model for understanding and interpreting the effects of normal aging in human brains. Unlike the short-lived rodents, for example, in monkeys the effects of aging extend over many years. Indeed, the life span of rhesus monkeys closely approaches that of humans, since these monkeys live to a maximum of about 35 years. So that if humans are considered to live for about 100 years of age, then one monkey year is equivalent to about 3 human years. Another important consideration for studying the effects of normal aging on the brains of rhesus monkeys is these monkeys do not develop Alzheimer's disease, so that the effects of normal aging are not confounded by pathological changes that might occur during the early stages of Alzheimer's disease. Some senile plaques do occur in the cerebral cortices of rhesus monkeys, but the plaques are few in number and their frequency does not correlate with cognitive decline. Moreover, rhesus monkeys have complex behavior patterns that approach those of humans, so that behavioral tests similar to those used in humans can be employed to accurately assess their cognitive status before their brains are preserved for structural evaluations. This means that determinations can be made about whether the frequency of occurrence of a particular age-related fine structural alteration does or does not correlate with cognitive decline. The brain tissue used in our studies has been fixed by perfusion of aldehyde containing solutions through the heart. Tissue blocks were then taken, osmicated and embedded in Araldite for thin sectioning. The thin sections were stained with lead citrate and uranyl acetate, before being photographed in an electron microscope. The 3×4” sheet film negatives were then scanned at high resolution and stored in a computer. The 130 electron micrographs in this website are presented in 18 chapters, each chapter being devoted to a particular component of the brain, and each chapter has a brief introduction to explain something about the images that are being presented within it. The images have minimal labeling, and some of the micrographs have colored versions. These colored versions show the distribution and relationships of the various components of the neuropil, and to help in interpretation of the images, as far as possible a standardized color scheme has been used throughout. Figures 1 and ​and22 show representative examples from this resource. Figure 1 Plate 14.5: A microglial cell in the primary visual cortex of a 35 year old monkey. Note the phagocytosed material at the two poles of the perikaryon (arrows). Figure 2 Plate 15.2: A large hole lying adjacent to a neuronal cell body in the neuropil of layer 3 in the primary visual cortex of a 35 year old monkey. This hole contains membranous debris and may represent a degenerating dendrite or neuronal cell body. It should be pointed out that to date very few parts of the non-human primate brain have been examined to determine the effects of normal aging on the central nervous system. And furthermore only a few studies have been carried out in which the tissue being examined is from primates that have been behaviorally tested to determine their cognitive status. As far as gray matter is concerned, aging studies have been largely confined to area 46 of the prefrontal cortex and to the primary visual cortex, area 17, with a few observations on dentate gyrus, and on the Betz cells in motor cortex. More is known about the effects of aging on white matter, since the fine structure of nerve fibers has been examined in a number of well-circumscribed fiber bundles in the cerebral hemispheres. Reviews of the results of these studies can be found in the reviews by Peters and Kemper (2012) and Morrison and Baxter (2012). A summary of what is known about the effects of aging on the morphological integrity of the primate brain is as follows: A number of structural factors, such as the total volume of the brain, the numbers of neurons, and astrocytes and microglial cells in various parts of the brain, do not appear to alter significantly with increasing age. Some structural alterations increase with frequency with age, but the frequency does not correlate with cognitive decline. Among these alterations are age-related losses of nerve fibers that are 20% or lower, and an increased frequency of degenerating myelin sheaths in some fiber tracts. Other alterations in this category are an increase in the frequency of senile plaques; an increase in frequency of oligodendrocytes; and the loss of synapses from the lower layers of the prefrontal cortex. Among the structural alterations that increase in frequency with age, and the frequency of which correlate with cognitive decline, are the following: an increased frequency of degenerating myelin sheaths, the loss of substantial numbers of nerve fibers from some fiber tracts, and the loss of synapses and dendritic spines from the upper layers of prefrontal area 46. What is becoming clear is that the cognitive decline that occurs during normal aging is not attributable to a single factor, and that while degenerative alterations are occurring some repair is also taking place. The most obvious example of repair is the remyelination that leads to the formation of more numerous and shorter internodal lengths of myelin, and the increased numbers of oligodendrocytes that are generated to effect this repair. Obviously, this is only a beginning in our understanding the effects of aging on the primate brain. In the future, additional cortical areas need to be examined to determine if alterations, such as the synapse losses from the upper layers of area 46 of the cortex, are specific to that area or whether synaptic losses occur throughout the cortex. If synaptic losses are ubiquitous, the origins of the axon terminals that degenerate to account for the losses must be determined.

Journal ArticleDOI
TL;DR: While there were significant differences among species, phylogenetic trends in NPY‐ir neuron distributions were not observed and humans did not differ from other primates, however, variation among species warrants further investigation into the distribution of this neuromodulator system.
Abstract: We examined the distribution of neurons immunoreactive for neuropeptide Y (NPY) in the posterior part of the superior temporal cortex (Brodmann's area 22 or area Tpt) of humans and nonhuman haplorrhine primates. NPY has been implicated in learning and memory and the density of NPY-expressing cortical neurons and axons is reduced in depression, bipolar disorder, schizophrenia, and Alzheimer's disease. Due to the role that NPY plays in both cognition and neurodegenerative diseases, we tested the hypothesis that the density of cortical and interstitial neurons expressing NPY was increased in humans relative to other primate species. The study sample included great apes (chimpanzee and gorilla), Old World monkeys (pigtailed macaque, moor macaque, and baboon) and New World monkeys (squirrel monkey and capuchin). Stereologic methods were used to estimate the density of NPY-immunoreactive (-ir) neurons in layers I-VI of area Tpt and the subjacent white matter. Adjacent Nissl-stained sections were used to calculate local densities of all neurons. The ratio of NPY-ir neurons to total neurons within area Tpt and the total density of NPY-ir neurons within the white matter were compared among species. Overall, NPY-ir neurons represented only an average of 0.006% of the total neuron population. While there were significant differences among species, phylogenetic trends in NPY-ir neuron distributions were not observed and humans did not differ from other primates. However, variation among species warrants further investigation into the distribution of this neuromodulator system.

Journal ArticleDOI
TL;DR: Major differences in the organization of the vestibular brainstem among Old World anthropoid primate species are revealed and in chimpanzees, as well as humans, there is individual variability in the organizations of brainstem nuclei.
Abstract: Chimpanzees are one of the closest living relatives of humans. However, the cognitive and motor abilities of chimpanzees and humans are quite different. The fact that humans are habitually bipedal and chimpanzees are not implies different uses of vestibular information in the control of posture and balance. Furthermore, bipedal locomotion permits the development of fine motor skills of the hand and tool use in humans, suggesting differences between species in the structures and circuitry for manual control. Much motor behavior is mediated via cerebro-cerebellar circuits that depend on brainstem relays. In this study, we investigated the organization of the vestibular brainstem in chimpanzees to gain insight into whether these structures differ in their anatomy from humans. We identified the four nuclei of vestibular nuclear complex in the chimpanzee and also looked at several other precerebellar structures. The size and arrangement of some of these nuclei differed between chimpanzees and humans, and also displayed considerable inter-individual variation. We identified regions within the cytoarchitectonically defined medial vestibular nucleus visualized by immunoreactivity to the calcium-binding proteins calretinin and calbindin as previously shown in other species including human. We have found that the nucleus paramedianus dorsalis, which is identified in the human but not in macaque monkeys, is present in the chimpanzee brainstem. However, the arcuate nucleus, which is present in humans, was not found in chimpanzees. The present study reveals major differences in the organization of the vestibular brainstem among Old World anthropoid primate species. Furthermore, in chimpanzees, as well as humans, there is individual variability in the organization of brainstem nuclei.

Journal ArticleDOI
10 Sep 2013-PeerJ
TL;DR: Orangutans matched images from both category levels spontaneously whereas the gorilla showed effects of learning to match intermediate level categories, showing that biological knowledge is not necessary to form natural categories at both concrete and intermediate levels.
Abstract: Following a series of experiments in which six orangutans and one gorilla discriminated photographs of different animal species in a two-choice touch screen procedure, Vonk & MacDonald (2002) and Vonk & MacDonald (2004) concluded that orangutans, but not the gorilla, seemed to learn intermediate level category discriminations, such as primates versus non-primates, more rapidly than they learned concrete level discriminations, such as orangutans versus humans. In the current experiments, four of the same orangutans and the gorilla were presented with delayed matching-to-sample tasks in which they were rewarded for matching photos of different members of the same primate species; golden lion tamarins, Japanese macaques, and proboscis monkeys, or family; gibbons, lemurs (Experiment 1), and subsequently for matching photos of different species within the following classes: birds, reptiles, insects, mammals, and fish (Experiment 2). Members of both Great Ape species were rapidly able to match the photos at levels above chance. Orangutans matched images from both category levels spontaneously whereas the gorilla showed effects of learning to match intermediate level categories. The results show that biological knowledge is not necessary to form natural categories at both concrete and intermediate levels.

Journal ArticleDOI
TL;DR: The sex‐specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis) is described and it is hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.
Abstract: Offspring size is often an intimate link between the fitness of parents and offspring. Among mammals, neonate mass is also related to adult levels of dimorphism and intrasexual competitive mating. We describe the sex-specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis), a small Neotropical primate. Best fitting quantitative genetic models show strong maternal genetic effects with little difference between sexes offering limited opportunity for neonatal dimorphism to respond to observed or hypothetical selection. Heritabilities that are approximately zero also imply it is unlikely that neonatal dimorphism can evolve as a correlated response to selection on adult size. However, male mass is also more dependent on maternal condition (age and parity) making dimorphism plastic. Finally, we hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.

Journal ArticleDOI
TL;DR: The interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities.

Journal ArticleDOI
TL;DR: The study highlights the fact that differences in cognitive abilities do not always map neatly onto phylogenetic relationships and that in a number of cognitive experiments monkeys do not fare significantly worse than apes, casting doubt on the assumption that larger brains per se confer an advantage in such kinds of tests.
Abstract: Whether the cognitive competences of monkeys and apes are rather similar or whether the larger-brained apes outperform monkeys in cognitive experiments is a highly debated topic. Direct comparative analyses are therefore essential to examine similarities and differences among species. We here compared six primate species, including humans, chimpanzees, bonobos, gorillas (great apes), olive baboons, and long-tailed macaques (Old World monkeys) in a task on fine-grained size discrimination. Except for gorillas, subjects of all taxa (i.e. humans, apes, and monkeys) were able to discriminate three-dimensional cubes with a volume difference of only 10 % (i.e. cubes of 50 and 48 mm side length) and performed only slightly worse when the cubes were presented successively. The minimal size discriminated declined further with increasing time delay between presentations of the cubes, highlighting the difficulty to memorize exact size differences. The results suggest that differences in brain size, as a proxy for general cognitive abilities, did not account for variation in performance, but that differential socio-ecological pressures may better explain species differences. Our study highlights the fact that differences in cognitive abilities do not always map neatly onto phylogenetic relationships and that in a number of cognitive experiments monkeys do not fare significantly worse than apes, casting doubt on the assumption that larger brains per se confer an advantage in such kinds of tests.

Book ChapterDOI
01 Jan 2013
TL;DR: This chapter sketches out the historical transformations in this long and fraught relationship between the people and monkeys of Japan in an attempt to identify a few crucial values that have characterized the intimate yet conflicted attitude of the Japanese people toward a fellow primate species with which they share a habitat.
Abstract: The ancestors of both the Japanese monkey (Macaca fuscata) and humans (Homo sapiens) arrived in the Japanese archipelago during the Pleistocene epoch. Thus, humans and monkeys have lived together in Japan for more than 35,000 years. This chapter sketches out the historical transformations in this long and fraught relationship between the people and monkeys of Japan in an attempt to identify a few crucial values that we believe have characterized the intimate yet conflicted attitude of the Japanese people toward a fellow primate species with which they share a habitat. From the neolithic, monkeys were hunted for food or were venerated for their spiritual powers. Today, monkeys have become subjects of scientific research into their natural ecology as well as for the management of their populations. While nature conservation policy may be mainly the work of scientists and the government, it is important that Japanese people continue their relationship with monkeys as neighbors with their own personalities, based on a culture of “anthropomorphized personalities.” The solutions to wildlife issues need to be formulated within the cultural context of each place where humans and primates coexist.

Journal ArticleDOI
TL;DR: The results of a six-month long study of the feeding preferences and ranging patterns of the Yucatan spider monkey Ateles geoffroyi yucatanensis living in the "Yaaxche" reserve by the Caribbean coast in northeastYucatan peninsula are reported.
Abstract: The spider monkey, a fruit specialist and important seed dispersal agent in the Neotropics, is an endangered primate due to habitat loss, hunting and the pet trade. Spider monkeys have been the subject of a few studies in Central and South Ame- rica, but little is known about the diet and ranging for this primate in southern Mexico. Here we report the results of a six-month long study (October 2010 to March 2011) of the feeding preferences and ranging patterns of the Yucatan spider monkey Ateles geoffroyi yucatanensis living in the "Yaaxche" reserve by the Caribbean coast in northeast Yucatan peninsula. Focal animal and scan sampling as well as GPS tracking were used to document spider monkey feeding behavior, location of food trees and ranging in the reserve. The spider monkeys used 36 species of plants (94% trees; n = 432) and six non tree morphospecies as a source of food. Six tree species accounted for ≥80% of total feeding time and for 74% of all trees used. Fruits accounted for 59% of total feeding time, followed by leaves (35%), palm piths (5%) and other plant parts (1%). Total range used by the monkeys was esti- mated at 43% of semievergreen rainforest habitat available (ca 40ha). Range use was not random with segments showing light, moderate and heavy use; the use of different areas of their range varied monthly and was closely linked to the spatial dispersion of the trees used for food (Current Zoology 59 (1): 125-134, 2013).

01 Jan 2013
TL;DR: The functional response in the seed predation behavior to fruiting seasonality of red leaf monkeys in Danum Valley, Sabah, northern Borneo demonstrated a functional response to mast fruiting, but found no support for the predator satiation hypothesis.
Abstract: The predator satiation hypothesis is one plausible explanation for masting in lowland dipterocarp forests in SE Asia. Hence, evaluation of behavioral patterns of seed predators have the potential to provide support fo r the predator satiation hypothesis. In order to evaluate possible mechanisms that could result in predator satiation, we studied the functional response in the seed predation behavior to fruiting seasonality of red leaf monkeys ( Presbytis rubicunda MA¼ller, 1838, Colobinae) in Danum Valley, Sabah, northern Borneo. Specifically, we sought to answer the two questions: (1) when fruit availability increases, to what extent do red leaf monkeys increase their seed eating? and (2) do red leaf monkeys change the degree to which they pursue one species of seeds in respon se to the changes in community-level fruit availability? In response to the increased fruit availability, red leaf monkeys extended their time spent feeding on seeds as much as 18 fold. This large functional response resulted from the elongated total feeding time and the preference for seeds by red leaf monkeys. Feeding time tended to increase, up to 28 % of the observation time, with increasing fruit availability. In response to increased fruiting seasonality, the monkeys increased the number of species and plant individuals upon whose seeds they depredated. Time spent feeding on seeds per species or individual, or for the most frequently eaten species or individual, was not affected by fruit availability. Similarly, the duration of one seed-feeding event was unaffected by the fruit availability. Hence, while our results demonstrate a functional response to mast fruiting, we found no support for the predator satiation hypothesis. The existence of an abundant alternative resource (young leaves) is one of several likely reasons for the weak persistence toward seeds shown by red leaf monkeys, whic h is contradictory to the assumption of the predator satiation hypothesis.

Journal ArticleDOI
TL;DR: Capuchins were initially less accurate than rhesus in Study 2, but with experience, achieved similar accuracy rates and presentation durations, indicating that rapid visual processing abilities are widespread in the primate lineage, and that the form of the stimuli presented can have an effect on processing across species.
Abstract: Visual acuity is a defining feature of the primates. Humans can process visual stimuli at extremely rapid presentation durations, as short as 14 ms. Evidence suggests that other primates, including chimpanzees and rhesus macaques, can process visual information at similarly rapid rates. What is lacking is information on the abilities of New World monkeys, which is necessary to determine whether rapid processing is present across the primates or is specific to Old World primates. We tested capuchin (Cebus apella) and rhesus (Macaca mulatta) monkeys on a computerized matching-to-sample paradigm to determine the shortest presentation duration at which stimuli could be correctly identified. In Study 1, using clip art images, both species achieved presentation durations as short as 25 ms while maintaining high accuracy rates. In Study 2, we used logographic Asian language characters to see if stimuli that were more similar in appearance would reveal species differences. Neither species was as accurate, or achieved as short of presentation durations, as with clip-art images. In particular, capuchins were initially less accurate than rhesus in Study 2, but with experience, achieved similar accuracy rates and presentation durations. These data indicate that rapid visual processing abilities are widespread in the primate lineage, and that the form of the stimuli presented can have an effect on processing across species.

Dissertation
13 Sep 2013
TL;DR: This thesis illustrates the potential use of GC measurements as a tool to monitor populations in disturbed areas and demonstrates that interdisciplinary research could improve conservation efforts, which will be necessary to ensure the conservation of the global biodiversity.
Abstract: The increasing intensity of anthropogenic land use and conversion has immense impacts on ecosystems worldwide and often results in habitat fragmentation. Fragmentation and other anthropogenic disturbances (e.g. hunting and logging activities) pose major threats to numerous animal species. Species vary greatly in their resilience to these disturbances and in their ability to survive in forest fragments. Animals might have to adjust their behavior, their grouping patters and/or dietary strategies to survive. Human-induced alterations can also result in long-term elevations of ‘stress’ hormones (glucocorticoids), which can have deleterious effects on growth, reproduction and immune system activity of animals. In this thesis I applied an interdisciplinary approach and combined behavioral observations with data on fecal glucocorticoid metabolite (FGCM) levels. To broaden our understanding of how animals cope physiologically and behaviorally with anthropogenic disturbances I studied two Neotropical primate species, brown spider monkeys (Ateles hybridus) and red howler monkeys (Alouatta seniculus). I collected fecal samples in several fragments in Colombia that differed in size (4.21 ha - 500 ha) as well as the level of human impact (determined through the occurrence and/or absence of hunting and logging activities). Using a previously validated enzymeimmunoassay I examined species-specific differences in the physiological responsiveness to both factors. Fragment size did not influence FGCM levels of either species. But spider monkeys showed elevated FGCM levels in fragments where both hunting and logging occurred, whereas howler monkeys did not show such a response. This suggests that hunting and logging activities might create long-term elevations of GC levels in spider monkeys and emphasizes why they are at a higher extinction risk than howler monkeys when living in anthropogenically altered habitats. To better understand how spider monkeys cope with fragmentation, I investigated how two groups modify their flexible grouping patterns and social behavior in a small fragment (65 ha). I collected data on subgroup sizes, aggression, habitat-wide fruit availability and collected fecal samples to determine FGCM levels. Both groups ranged in smaller subgroups and showed higher FGCM levels when fruit availability was high compared to when it was low. This was unexpected because (1) primate species that exhibit fission-fusion dynamics typically show the opposite grouping pattern and (2) a major function of glucocorticoids (GC) is the release of energy during the stress response. Consequently, GC levels typically increase in times of low resource availability. Spider monkeys are generally considered to be ripe fruit specialists. However, both groups have a more folivorous diet than other spider monkey populations. This seems to be a way to reduce the level of competition for fruit in times of low availability. When fruit availability is relatively high in this fragment it appears that the intra-group feeding competition for fruit is also high. This would also explain why FGCM levels were higher and subgroup size smaller in times of high fruit availability. This is further reinforced by unusually high levels, for spider monkeys, of female-female aggression, which was also more often observed when fruit availability was high. This illustrates how fragmentation can change the ability of spider monkeys to decrease intra-group feeding competition via flexible grouping patterns and that the relationship between resource availability, grouping patterns, aggression rates and stress levels can be more complex than assumed so far. In conclusion, this study demonstrates species-specific differences in the ability to cope with anthropogenic disturbances and that these differences can be, at least partly, attributed to different levels of physiological responsiveness. Importantly, this thesis illustrates the potential use of GC measurements as a tool to monitor populations in disturbed areas and it demonstrates that interdisciplinary research could improve conservation efforts, which will be necessary to ensure the conservation of the global biodiversity.


Journal ArticleDOI
TL;DR: This paper reviewed the distribution, genotype, expression and restriction mechanism for inhibiting retroviruses replication of TRIMCyp fusion gene in primates and found that they may play very important roles in restricting HIV-1 replication and determine the susceptibility to HIV- 1 infection.
Abstract: TRIM5-cyclophilin A (TRIMCyp) fusion gene is an unusual TRIM5 locus. At present, this fusion phenomenon has been found in the representative species which contain owl monkey (Aotus trivirgatus) of Aotus genus that belongs to New World monkeys and Old World monkeys such as Northern pig-tailed macaque (M. leonina), Sunda pig-tailed macaque(M. nemestrina), Crab-eating macaque (M. fascicularis), Indian rhesus macaque (M. mulatta) and Assam macaque (M. assamensis), etc. But the fusion mode and transcription splicing pattern of TRIMCyp fusion gene are different between New World and Old World monkeys. The TRIMCyp fusion gene of New World monkeys is formed by inserting a CypA pseudogene cDNA sequence into the region between exon 7 and exon 8 of the TRIM5 locus through retrotransposition. However the TRIMCyp fusion gene of Old World monkeys results from the retrotransposition of a CypA pseudogene cDNA into 3' terminal or 3'-UTR of TRIM5 gene. The distributions, genotypes, expression and restricting activities against different retroviruses of TRIMCyp were different across species of primates. Moreover, most of the researches focused on the TRIMCyp fusion gene of owl monkey and pig-tailed macaque and found that they may play very important roles in restricting HIV-1 replication and determine the susceptibility to HIV-1 infection. It was reported that the TRIMCyp protein of owl monkey could inhibit HIV-1 infection in a similar way as TRIM5α, but TRIMCyp protein of pig-tailed monkey loss the restricting activity to HIV-1 infection. Here we reviewed the distributions, genotypes and restriction mechanism for inhibiting retroviruses replication of TRIMCyp fusion gene in primates.