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Showing papers on "Primate published in 2019"


Journal ArticleDOI
TL;DR: The generation of BMAL1 knockout cynomolgus monkeys for circadian-related disorders by CRISPR/Cas9 editing of monkey embryos are reported, showing higher nocturnal locomotion and reduced sleep and defective sensory processing in auditory oddball tests found in schizophrenia patients.
Abstract: Circadian disruption is a risk factor for metabolic, psychiatric and age-related disorders, and non-human primate models could help to develop therapeutic treatments. Here, we report the generation of BMAL1 knockout cynomolgus monkeys for circadian-related disorders by CRISPR/Cas9 editing of monkey embryos. These monkeys showed higher nocturnal locomotion and reduced sleep, which was further exacerbated by a constant light regimen. Physiological circadian disruption was reflected by the markedly dampened and arrhythmic blood hormonal levels. Furthermore, BMAL1-deficient monkeys exhibited anxiety and depression, consistent with their stably elevated blood cortisol, and defective sensory processing in auditory oddball tests found in schizophrenia patients. Ablation of BMAL1 up-regulated transcriptional programs toward inflammatory and stress responses, with transcription networks associated with human sleep deprivation, major depressive disorders, and aging. Thus, BMAL1 knockout monkeys are potentially useful for studying the physiological consequences of circadian disturbance, and for developing therapies for circadian and psychiatric disorders.

81 citations


Journal ArticleDOI
TL;DR: Neuroimaging data from the brains of humans, chimpanzees, baboons, and macaques are used to reveal shared and distinct sulcal morphology of the medial frontal cortex, leading to clear predictions about how other primate brains might be anatomo-functionally organized.
Abstract: Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of the human uniqueness, if any, and between-species anatomo-functional comparisons of the frontal areas remain controversial. To provide a novel interpretation of the evolution of primate brains, sulcal morphological variability of the medial frontal cortex was assessed in Old World monkeys (macaque/baboon) and Hominoidea (chimpanzee/ human). We show that both Hominoidea possess a paracingulate sulcus, which was previously thought to be unique to the human brain and linked to higher cognitive functions, such as mentalizing. Also, we show systematic sulcal morphological organization of the medial frontal cortex that can be traced from Old World monkeys to Hominoidea species, demonstrating an evolutionarily conserved organizational principle. These data provide a new framework to compare sulcal morphology, cytoarchitectonic areal distribution, connectivity, and function across the primate order, leading to clear predictions about how other primate brains might be anatomo-functionally organized.

63 citations


Journal ArticleDOI
TL;DR: The turbinal morphology of Rooneyia viejaensis, a late middle Eocene primate of uncertain phylogenetic affinities from the Tornillo Basin of West Texas, is described and it is suggested that although Rooneyia was broadly plesiomorphic in retaining a large complement of olfactory turbinals as in living strepsirrhines, Rooneyia may have evolved somewhat diminished Olfactory abilities as inliving haplorhines.

47 citations


Journal ArticleDOI
TL;DR: It is demonstrated that the SCNT approach could be used to generate cloned monkeys from fibroblasts of a young adult monkeys and paves the way for the development of macaque monkey disease models with uniform genetic backgrounds.
Abstract: Cloning of macaque monkeys by somatic cell nucleus transfer (SCNT) allows the generation of monkeys with uniform genetic backgrounds that are useful for the development of non-human primate models of human diseases. Here, we report the feasibility of this approach by SCNT of fibroblasts from a macaque monkey (Macaca fascicularis), in which a core circadian transcription factor BMAL1 was knocked out by clustered regularly interspaced short palindromic repeat/Cas9 gene editing (see accompanying paper). Out of 325 SCNT embryos transferred into 65 surrogate monkeys, we cloned five macaque monkeys with BMAL1 mutations in both alleles without mosaicism, with nuclear genes identical to that of the fibroblast donor monkey. Further peripheral blood mRNA analysis confirmed the complete absence of the wild-type BMAL1 transcript. This study demonstrates that the SCNT approach could be used to generate cloned monkeys from fibroblasts of a young adult monkeys and paves the way for the development of macaque monkey disease models with uniform genetic backgrounds.

47 citations


Journal ArticleDOI
TL;DR: The results suggest that the functional organization of the motor cortex represents not just muscles of the body, but muscle synergies that form the building blocks of the complex behavioral repertoire of these animals.
Abstract: In the present study, we investigated motor cortex (M1) and a small portion of premotor and parietal cortex using intracortical microstimulation in anesthetized capuchin monkeys. Capuchins are the only New World monkeys that have evolved an opposable thumb and use tools in the wild. Like most Old World monkeys and humans, capuchin monkeys have highly dexterous hands. We surveyed a large extent of M1 and found that ~22% of all evoked movements in M1 involved the digits, and the majority of these consisted of finger flexions and extensions. Different subtypes of movements could be identified, including opposable movements of digits 1 and 2 (D1 and D2). Interestingly, the pattern of such movements varied between animals. In one case, movements involved the adduction of the medial surface of D1 toward the lateral surface of D2, whereas in the other case, the tips of D1 and D2 came in contact. Unlike other primates examined, we also found extensive representations of the prehensile foot and tail. We propose that the manual behavioral repertoire of capuchin monkeys, which includes the use of tools in the wild, is well represented within the motor cortex in the form of muscle synergies between different body parts that compose these larger, complex behaviors.SIGNIFICANCE STATEMENT The ability to use tools is a milestone in human evolution. Capuchin monkeys are one of the few non-human primates that use tools in the wild. The present study is the first detailed exploration of the motor cortex of these primates using long-train intracortical microstimulation. Within primary motor cortex, we evoked finger movements involving flexions and extensions of multiple digits, or of the first and second digits alone. Interestingly, flexion of tail and toes could also be evoked. Together, these results suggest that the functional organization of the motor cortex represents not just muscles of the body, but muscle synergies that form the building blocks of the complex behavioral repertoire of these animals.

25 citations


Journal ArticleDOI
TL;DR: The common marmoset, a New World (platyrrhine) monkey, is currently being fast-tracked as a non-human primate model species, especially for genetic modification but also as a general-purpose model for research on the brain and behavior bearing on the human condition.
Abstract: The common marmoset, a New World (platyrrhine) monkey, is currently being fast-tracked as a non-human primate model species, especially for genetic modification but also as a general-purpose model for research on the brain and behavior bearing on the human condition. Compared to the currently dominant primate model, the catarrhine macaque monkey, marmosets are notable for certain evolutionary specializations, including their propensity for twin births, their very small size (a result of phyletic dwarfism), and features related to their small size (rapid development and relatively short lifespan), which result in these animals yielding experimental results more rapidly and at lower cost. Macaques, however, have their own advantages. Importantly, macaques are more closely related to humans (which are also catarrhine primates) than are marmosets, sharing approximately 20 million more years of common descent, and are demonstrably more similar to humans in a variety of genomic, molecular, and neurobiological characteristics. Furthermore, the very specializations of marmosets that make them attractive as experimental subjects, such as their rapid development and short lifespan, are ways in which marmosets differ from humans and in which macaques more closely resemble humans. These facts warrant careful consideration of the trade-offs between convenience and cost, on the one hand, and biological realism, on the other, in choosing between non-human primate models of human biology. Notwithstanding the advantages marmosets offer as models, prudence requires continued commitment to research on macaques and other primate species.

24 citations


Journal ArticleDOI
TL;DR: The findings suggest that the clearer segregation observed in the human frontal pole reflects regional differences already present in early simian primates, and that overall brain mass influences the pattern of cortico-cortical connectivity.
Abstract: Area 10, located in the frontal pole, is a unique specialization of the primate cortex. We studied the cortical connections of area 10 in the New World Cebus monkey, using injections of retrograde tracers in different parts of this area. We found that injections throughout area 10 labeled neurons in a consistent set of areas in the dorsolateral, ventrolateral, orbital, and medial parts of the frontal cortex, superior temporal association cortex, and posterior cingulate/retrosplenial region. However, sites on the midline surface of area 10 received more substantial projections from the temporal lobe, including clear auditory connections, whereas those in more lateral parts received >90% of their afferents from other frontal areas. This difference in anatomical connectivity reflects functional connectivity findings in the human brain. The pattern of connections in Cebus is very similar to that observed in the Old World macaque monkey, despite >40 million years of evolutionary separation, but lacks some of the connections reported in the more closely related but smaller marmoset monkey. These findings suggest that the clearer segregation observed in the human frontal pole reflects regional differences already present in early simian primates, and that overall brain mass influences the pattern of cortico-cortical connectivity.

23 citations


Journal ArticleDOI
TL;DR: It is found that juveniles viewed stimuli more than other age groups, videos were viewed more than static photo imagery, and that monkeys increased their viewing time when presented with multiple eye tracking sessions.
Abstract: Eye-tracking methods measure what humans and other animals visually attend to in the environment. In nonhuman primates, eye tracking can be used to test hypotheses about how primates process social information. This information can further our understanding of primate behavior as well as offer unique translational potential to explore causes of or treatments for altered social processing as seen in people with neurodevelopmental disorders such as autism spectrum disorder and schizophrenia. However, previous methods for collecting eye-tracking data in nonhuman primates required some form of head restraint, which limits the opportunities for research with respect to the number of or kinds of primates that can undergo an eye-tracking study. We developed a novel, noninvasive method for collecting eye tracking data that can be used both in animals that are difficult to restrain without sedation as well as animals that are of different ages and sizes as the box size can be adjusted. Using a transport box modified with a viewing window, we collected eye-tracking data in both New (Callicebus cupreus) and Old World monkeys (Macaca mulatta) across multiple developmental time points. These monkeys had the option to move around the box and avert their eyes from the screen, yet, they demonstrated a natural interest in viewing species-specific imagery with no previous habituation to the eye-tracking paradigm. Provided with opportunistic data from voluntary viewing of stimuli, we found that juveniles viewed stimuli more than other age groups, videos were viewed more than static photo imagery, and that monkeys increased their viewing time when presented with multiple eye tracking sessions. This noninvasive approach opens new opportunities to integrate eye-tracking studies into nonhuman primate research.

23 citations


Journal ArticleDOI
TL;DR: The attitudes of rural residents towards monkeys in Sri Lanka were surveyed and evaluated in an effort to contribute to an ethnoprimatological approach to conservation, i.e., promote a coexistence and sharing of habitat between humans and monkeys.
Abstract: Sri Lanka is a biodiversity hotspot with high human density that contributes to increasing human-monkey conflict (HMC). In 50 years of primate studies there, the development of HMC has been documented, and many workshops and interventions organized to ameliorate HMC. These activities prompted the present survey. In the extensive lowland dry zone of Sri Lanka, the affected nonhuman primates are the toque macaque, gray and purple-faced langurs and slender loris. We surveyed and evaluated the attitudes of rural residents towards these four species in an effort to contribute to an ethnoprimatological approach to conservation, i.e., promote a coexistence and sharing of habitat between humans and monkeys. We selected 13 villages near Polonnaruwa, located centrally in the dry zone. The four nonhuman primate species differ in their behavioral ecologies, and this influenced how frequently they were thought of as pests. Most HMC was with the macaque and gray langur, less with the purple-faced langur and least with the loris. The underlying sentiment among stakeholders towards monkeys was generally either neutral or positive. Nonetheless, the majority (80%) of people desired a translocation of the troublesome monkeys from their properties to protected areas, which is impractical. Few (< 1%) openly wanted monkeys destroyed. While a traditional reverence for monkeys provides a solid basis for science and media-based education, it also contributes to the feeding of monkeys and consequent unnatural population growth, and enhanced HMC. Public understanding of the underlying causes of HMC was poor, hindering effective solutions. A combination of a feeding ban, possibly contraceptive intervention at localized HMC trouble spots, and extensive education may be the only benign alternatives to the destruction of wild primates by a powerful minority. Coexistence through strengthening and expansion of exclusive suitable protected habitats for all wildlife is a priority.

19 citations


Journal ArticleDOI
TL;DR: The simple dentition and absence of bilophodonty in the Nakwai monkey indicate that the initial radiation of Old World monkeys was first characterized by a reorganization of basic molar morphology, and a reliance on cusps rather than lophs suggests frugivorous diets and perhaps hard object feeding.
Abstract: Old World monkeys (Cercopithecoidea) are a highly successful primate radiation, with more than 130 living species and the broadest geographic range of any extant group except humans. Although cercopithecoids are highly variable in habitat use, social behavior, and diet, a signature dental feature unites all of its extant members: bilophodonty (bi: two, loph: crest, dont: tooth), or the presence of two cross-lophs on the molars. This feature offers an adaptable Bauplan that, with small changes to its individual components, permits its members to process vastly different kinds of food. Old World monkeys diverged from apes perhaps 30 million years ago (Ma) according to molecular estimates, and the molar lophs are sometimes incompletely developed in fossil species, suggesting a mosaic origin for this key adaptation. However, critical aspects of the group's earliest evolution remain unknown because the cercopithecoid fossil record before ∼18 Ma consists of only two isolated teeth, one from Uganda and one from Tanzania. Here we describe a primitive Old World monkey from Nakwai, Kenya, dated at ∼22 Ma, that offers direct evidence for the initial key steps in the evolution of the cercopithecoid dentition. The simple dentition and absence of bilophodonty in the Nakwai monkey indicate that the initial radiation of Old World monkeys was first characterized by a reorganization of basic molar morphology, and a reliance on cusps rather than lophs suggests frugivorous diets and perhaps hard object feeding. Bilophodonty evolved later, likely in response to the inclusion of leaves in the diet.

18 citations


Journal ArticleDOI
TL;DR: This first study to directly compare visual recognition memory in two primate species—rhesus macaques and marmoset monkeys—on the same visual preferential looking task as a first step toward identifying similarities and differences in this cognitive process across the primate phylogeny is performed.
Abstract: The core functional organization of the primate brain is remarkably conserved across the order, but behavioral differences evident between species likely reflect derived modifications in the underlying neural processes. Here, we performed the first study to directly compare visual recognition memory in two primate species-rhesus macaques and marmoset monkeys-on the same visual preferential looking task as a first step toward identifying similarities and differences in this cognitive process across the primate phylogeny. Preferences in looking behavior on the task were broadly similar between the species, with greater looking times for novel images compared with repeated images as well as a similarly strong preference for faces compared with other categories. Unexpectedly, we found large behavioral differences among the two species in looking behavior independent of image familiarity. Marmosets exhibited longer looking times, with greater variability compared with macaques, regardless of image content or familiarity. Perhaps most strikingly, marmosets shifted their gaze across the images more quickly, suggesting a different behavioral strategy when viewing images. Although such differences limit the comparison of recognition memory across these closely related species, they point to interesting differences in the mechanisms underlying active vision that have significant implications for future neurobiological investigations with these two nonhuman primate species. Elucidating whether these patterns are reflective of species or broader phylogenetic differences (e.g., between New World and Old World monkeys) necessitates a broader sample of primate taxa from across the Order.

Journal ArticleDOI
TL;DR: The results suggest that, like capuchins, squirrel monkeys coordinate their behavior with others, suggesting that such mutual outcomes occur in at least some contexts, even in species that do not routinely cooperate.
Abstract: Games from experimental economics have provided insights into the evolutionary roots of social decision making in primates and other species. Multiple primate species' abilities to cooperate, coordinate and anti-coordinate have been tested utilizing variants of these simple games. Past research, however, has focused on species known to cooperate and coordinate in the wild. To begin to address the degree to which cooperation and coordination may be a general ability that manifests in specific contexts, the present study assessed the decisions of squirrel monkeys (Saimiri boliviensis; N = 10), a species not known for their cooperative behavior in these games. Pairs of monkeys were presented with the Assurance Game (a coordination game), the Hawk-Dove Game (an anti-coordination game) and the Prisoner's Dilemma (a cooperation game with a temptation to defect). We then compared squirrel monkeys' performance to existing data on capuchin monkeys (Sapajus [Cebus] apella), a closely related species that routinely cooperates, to determine what, if any, differences in decision making emerged. Some pairs of both species found the payoff-dominant Nash Equilibrium (NE) in the coordination game, but failed to find the NE in subsequent games. Our results suggest that, like capuchins, squirrel monkeys coordinate their behavior with others, suggesting that such mutual outcomes occur in at least some contexts, even in species that do not routinely cooperate.

Journal ArticleDOI
TL;DR: Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes, suggesting that different bacterial communities may be selected for as the infant ages.
Abstract: Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut-brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high-throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.

Journal ArticleDOI
TL;DR: Refining training for monkeys in neuroscience is essential to optimise their welfare and pair- or group-training monkeys helps acclimate them quicker to transport devices.

Journal ArticleDOI
TL;DR: In this article, the authors assessed temporal changes in landscape structure in the Lacandona rainforest, Mexico, and how these changes relate to population trends of black howler monkeys (Alouatta pigra).
Abstract: Non-human primates are among the most threatened mammals on Earth. Although some species, such as howler monkeys, are thought to be resistant to initial phases of habitat disturbance, the lack of longitudinal studies prevents determining if this holds over time. We assessed temporal changes in landscape structure in the Lacandona rainforest, Mexico, and how these changes relate to population trends of black howler monkeys (Alouatta pigra). We surveyed primates in 22 forest sites in 2011 and 2017, and related temporal changes in primate abundance and immature-to-female ratio with changes in the spatial structure of local landscapes (forest cover, matrix openness, number of forest patches, and forest edge density) using a multi-scale approach. Landscape changes occurring over a 6-year period were strongly associated with temporal changes in population parameters. Primate abundance increased as forest cover increased. Both primate abundance and immature-to-female ratio increased in sites located in landscapes where the number of patches increased over time, but where the proportion of open matrix decreased. Edge density showed a negative effect on immature-to-female ratio. This endangered primate might not be as tolerant to landscape disturbance as generally thought. Allowing forest patches to increase in number and/or size through active or passive restoration (reverse fragmentation), and preventing forest loss and an increase in matrix openness are key management strategies to preserve howler monkeys in this biodiversity hotspot.

Journal ArticleDOI
TL;DR: The laminar organization of V1 further supports the view that subl layers of layer 3 of primates have been commonly misidentified as sublayers of layer 4, and can usefully guide future studies of cortical connectivity and function.
Abstract: Mouse lemurs are the smallest of the living primates, and are members of the understudied radiation of strepsirrhine lemurs of Madagascar. They are thought to closely resemble the ancestral primates that gave rise to present day primates. Here we have used multiple histological and immunochemical methods to identify and characterize sensory areas of neocortex in four brains of adult lemurs obtained from a licensed breeding colony. We describe the laminar features for the primary visual area (V1), the secondary visual area (V2), the middle temporal visual area (MT) and area prostriata, somatosensory areas S1(3b), 3a, and area 1, the primary motor cortex (M1), and the primary auditory cortex (A1). V1 has "blobs" with "nonblob" surrounds, providing further evidence that this type of modular organization might have evolved early in the primate lineage to be retained in all extant primates. The laminar organization of V1 further supports the view that sublayers of layer 3 of primates have been commonly misidentified as sublayers of layer 4. S1 (area 3b) is proportionately wider than the elongated area observed in anthropoid primates, and has disruptions that may distinguish representations of the hand, face, teeth, and tongue. Primary auditory cortex is located in the upper temporal cortex and may include a rostral area, R, in addition to A1. The resulting architectonic maps of cortical areas in mouse lemurs can usefully guide future studies of cortical connectivity and function.

Journal ArticleDOI
TL;DR: It is shown that common marmosets, which are a highly prosocial species, discriminated between human actors who reciprocated in social exchanges and those who did not; however, Japanese monkeys, who are renowned for despotic social relationships, did not.
Abstract: Reciprocity and cooperation are fundamental to human society and are observed in nonhuman primates. Primates are not only sensitive to direct reciprocity and its violation but also indirect reciprocity. Recent studies demonstrated that some primate species adjusted their behavior by observing others' interactions. Capuchin, marmoset, and squirrel monkeys avoided taking food from human actors who behaved nonreciprocally; however, no such empirical evidence among Old World monkeys is available. Here, we show that common marmosets, which are a highly prosocial species, discriminated between human actors who reciprocated in social exchanges and those who did not; however, Japanese monkeys, who are renowned for despotic social relationships, did not. In the reciprocal condition, 2 human actors exchanged food equally, whereas in the nonreciprocal condition, 1 actor (nonreciprocator) ended up with all the food and the other actor with none. The common marmosets avoided receiving food from the nonreciprocator in the nonreciprocal condition. Nevertheless, the Japanese monkeys did not show differential preferences in either condition. These results suggest a crucial role for prosocial tendencies in monkeys' responses to asymmetric exchanges and indicate that third-party social evaluations are not homologous among primates. Further comparative studies with direct comparisons will be required to explore the underlying mechanism of third-party social evaluations. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Journal ArticleDOI
TL;DR: These findings suggest that forest loss has stronger negative effects on spider monkeys than forest fragmentation, especially in best-preserved rainforests, where monkeys may be pushed to use the matrix more frequently for feeding and/or traveling.
Abstract: Understanding population responses to landscape structure is critical to improve landscape planning. Yet, large uncertainty remains about how such responses vary among regions with different disturbance intensity. This knowledge is particularly important for forest-specialist species, such as spider monkeys. Assessing the effect of landscape composition and configuration on the abundance and reproductive success of spider monkeys (Ateles geoffroyi) in two fragmented rainforests with different land-use intensity. We calculated the encounter rate (relative abundance) and immature-to-female ratio (reproductive success) of spider monkeys in two Mexican rainforest regions (12 forest patches per region, ~ 1140 h of field observations), and assessed their responses to three landscape predictors (forest cover, matrix functionality, and forest patch density) considering the scale of effect in each region. Spider monkeys showed different responses to landscape structure in each region. Encounter rate increased strongly with matrix functionality in the more disturbed region, and tended to be negatively impacted by patch density in the best-preserved region, but this latter association was weak. Forest cover was positively related to immature-to-female ratio in both regions, but such association was stronger in the best-preserved region. Our findings suggest that forest loss has stronger negative effects on spider monkeys than forest fragmentation, especially in best-preserved rainforests. Matrix composition is relatively more important in more disturbed regions, where monkeys may be pushed to use the matrix more frequently for feeding and/or traveling. Preventing forest loss and improving matrix quality should be a priority for the conservation of this endangered species.

Journal ArticleDOI
TL;DR: The marmoset monkey represents a previously understudied position in the evolution of primate reach and grasp behavior and offers a unique composition of ancestral primate corticospinal organization combined with skilled hand use to explore the evolution and development of visually‐guided actions.
Abstract: Throughout the primate lineage, there is a wide diversity of prehensile capacity that is thought to stem from individual species foraging patterns. While many studies have explored primates with precise hand grips, such as higher apes, few have considered primates that lack opposition movements. The New World marmoset monkey occupies an intriguing niche, displaying adept control of their hand movements yet their absence of opposable digits results in relatively imprecise grasping actions when compared with those observed in Old World monkeys, apes, and humans. The marmoset monkey offers a unique composition of ancestral primate corticospinal organization combined with skilled hand use to explore the evolution and development of visually-guided actions. In this study, four adult marmosets were trained to perform a series of visually-guided tasks, designed to assess their control over locating and retrieving objects of differing dimensions. Two of these animals received a neonatal lesion of the inferior pulvinar (unilateral), a thalamic nucleus previously demonstrated to be involved in visuomotor development. The kinematics of their reaching and grasping patterns were recorded for offline analysis. Predictive modeling revealed that maximum grip aperture, time to reach peak velocity and hand use were reliable predictors of distinguishing between cohorts. A consistent feature observed across all tasks was that they do not precisely scale their grip according to the dimensions of the target object which may be attributed to their lack of independent digit control. Therefore, the marmoset monkey represents a previously understudied position in the evolution of primate reach and grasp behavior.

Journal ArticleDOI
TL;DR: In a free choice task, head-restrained marmosets prefer objects gazed at by a conspecific and, moreover, they exhibit considerably shorter choice reaction times for the same objects.
Abstract: The ability to extract the direction of the other’s gaze allows us to shift our attention to an object of interest to the other and to establish joint attention. By mapping one’s own intentions on the object of joint attention, humans develop a Theory of (the other’s) Mind (TOM), a functional sequence possibly disrupted in autism. Gaze following of both humans and old world monkeys is orchestrated by very similar cortical architectures, strongly suggesting homology. Also new world monkeys, a primate suborder that split from the old world monkey line about 35 million years ago, have complex social structures and one member of this group, the common marmosets (Callithrix jacchus) are known to follow human head-gaze. However, the question is if they use gaze following to establish joint attention with conspecifics. Here we show that this is indeed the case. In a free choice task, head-restrained marmosets prefer objects gazed at by a conspecific and, moreover, they exhibit considerably shorter choice reaction times for the same objects. These findings support the assumption of an evolutionarily old domain specific faculty shared within the primate order and they underline the potential value of marmosets in studies of normal and disturbed joint attention.

Journal ArticleDOI
TL;DR: The BCoM of primates is not more posteriorly located than in other quadrupedal mammals; however, there is a substantial range of variation in primates, from caudal (in arboreal quadrupeds) to cranial (in hominoids and terrestrial quadruped) positions.
Abstract: Objectives Whole body center of mass (BCoM) position values are lacking for a comparative sample of primates. Therefore, it still remains unknown whether the BCoM in primates is more posteriorly located than in other mammals. The aim of the present report is to provide data for a large sample of primate species and to compare the position of the BCoM in primates to non-primate mammals. Materials and methods We collected morphometrics on eight primate species belonging to various families: Hylobatidae (Nomascus grabriellae, Nomascus Siki), Cercopithecidae (Cercopithecus roloway, Cercopithecus lhoesti, Colobus guereza, Trachypithecus francoisi), Cebidae (Sapajus xanthosternos), and Atelidae (Ateles fusciceps). Using a geometric model, we assessed the position of the BCoM in a natural quadrupedal posture and in a control posture. To complete our comparative sample with a wider range of morphotypes, we added the data available in the literature for hominoids (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus, Hylobates lar) and another cercopithecoid species (Papio anubis). We also evaluated the phylogenetic signal of the position of the BCoM in primates. Results The variation in the position of the BCoM in primates is very large, ranging from 40% of the distance between the hip and the shoulder in Ateles fusciceps to 63% in Hylobates lar. We observed a strong phylogenetic signal for this trait: hominoid species, as well as the baboon, have a cranial BCoM relative to the midline between the hip and the shoulder, arboreal cercopithecoids and the spider monkey have a caudal BCoM, and the capuchin monkey has a BCoM positioned at mid-trunk. The variation observed in non-primate quadrupedal mammals lies inside the variation range of primates, from 51% in Felis catus to 63% in Canis familiaris. Discussion The BCoM of primates is not more posteriorly located than in other quadrupedal mammals; however, there is a substantial range of variation in primates, from caudal (in arboreal quadrupeds) to cranial (in hominoids and terrestrial quadrupeds) positions. This variation is related to a phylogenetic model that suggests stabilizing selection for this trait. It seems that the BCoM position mostly depends of the size of the appendicular system (i.e., limbs) and the tail. Therefore, it may also reflect a general trend in quadrupedal mammals with arboreal species exhibiting a caudal BCoM and terrestrial species exhibiting a cranial BCoM. These results are discussed in the context of the locomotor evolution of primates including locomotor habits and gait mechanics. We also propose a new "passive" mechanism for the explanation of the particular weight support pattern observed in primates with tails.

Journal ArticleDOI
TL;DR: Investigating the positivity rate of Plasmodium infection in free-living howler monkeys in an Atlantic Forest fragment in Joinville/SC found that infection must be monitored for the eco-epidemiological surveillance of malaria in the Atlantic Forest and during primate conservation program that involves the animal movement, such as translocations.
Abstract: BACKGROUND The influence of Plasmodium spp. infection in the health of Southern brown howler monkey, Alouatta guariba clamitans, the main reservoir of malaria in the Atlantic Forest, is still unknown. OBJECTIVES The aim of this study was to investigate the positivity rate of Plasmodium infection in free-living howler monkeys in an Atlantic Forest fragment in Joinville/SC and to associate the infection with clinical, morphometrical, haematological and biochemical alterations. METHODS Molecular diagnosis of Plasmodium infection in the captured monkeys was performed by Nested-polymerase chain reaction (PCR) (18S rRNA and coxI). Haematological and biochemical parameters were compared among infected and uninfected monkeys; clinical and morphometrical parameters were also compared. FINDINGS The positivity rate of Plasmodium infection was 70% among forty captured animals, the highest reported for neotropical primates. None statistical differences were detected in the clinical parameters, and morphometric measures comparing infected and uninfected groups. The main significant alteration was the higher alanine aminotransferase (ALT) levels in infected compared to uninfected monkeys. MAIN CONCLUSIONS Therefore, Plasmodium infection in howler monkeys may causes haematological/biochemical alterations which might suggest hepatic impairment. Moreover, infection must be monitored for the eco-epidemiological surveillance of malaria in the Atlantic Forest and during primate conservation program that involves the animal movement, such as translocations.

Journal ArticleDOI
TL;DR: Results from preferential viewing suggest that the hippocampus may be especially important for memory of incidentally encoded events, and passive memory tests that are not rewarded with food and that do not require extensive training may provide more sensitive measures of hippocampal function.
Abstract: Monkeys with selective damage to the hippocampus are often unimpaired in matching-to-sample tests but are reportedly impaired in visual paired comparison. While both tests assess recognition of previously seen images, delayed matching-to-sample may engage active memory maintenance whereas visual paired comparison may not. Passive memory tests that are not rewarded with food and that do not require extensive training may provide more sensitive measures of hippocampal function. To test this hypothesis, we assessed memory in monkeys with hippocampal damage and matched controls by providing them the opportunity to repeatedly view small sets of videos. Monkeys pressed a button to play each video. The same 10 videos were used for six consecutive days, after which 10 new videos were introduced in each of seven cycles of testing. Our measure of memory was the extent to which monkeys habituated with repeated presentations, watching fewer videos per session over time. Monkeys with hippocampal lesions habituated more slowly than did control monkeys, indicating poorer memory for previous viewings. Both groups dishabituated each time new videos were introduced. These results, like those from preferential viewing, suggest that the hippocampus may be especially important for memory of incidentally encoded events.

Posted ContentDOI
27 Jun 2019-bioRxiv
TL;DR: Common marmosets follow the head gaze of conspecifics in order to establish joint attention and this support the assumption of an evolutionary old domain specific faculty shared within the primate order and underline the potential value of marmoset in studies of normal and disturbed joint attention.
Abstract: The ability to extract the direction of the others gaze allows us to shift our attention to an object of interest to the other and to establish joint attention. By mapping ones own expectations, desires and intentions on the object of joint attention, humans develop a Theory of (the others) Mind (TOM), a functional sequence possibly disrupted in autism. Although old world monkeys probably do not possess a TOM, they follow the others gaze and they establish joint attention. Gaze following of both humans and old world monkeys fulfills Fodors criteria of a domain specific function and is orchestrated by very similar cortical architectures, strongly suggesting homology. Also new world monkeys, a primate suborder that split from the old world monkey line about 35 million years ago, have complex social structures. One member of this group, the common marmoset (Callithrix jacchus), has received increasing interest as a potential model in studies of normal and disturbed human social cognition. Marmosets are known to follow human head-gaze. However, the question is if they use gaze following to establish joint attention with conspecifics. Here we show that this is indeed the case. In a free choice task, head-restrained marmosets prefer objects gazed at by a conspecific and, moreover, they exhibit considerably shorter choice reaction times for the same objects. These findings support the assumption of an evolutionary old domain specific faculty shared within the primate order and they underline the potential value of marmosets in studies of normal and disturbed joint attention.nnHIGHLIGHTSO_LICommon marmosets follow the head gaze of conspecifics in order to establish joint attention.nC_LIO_LIBrief exposures to head gaze are sufficient to reallocate an animals attention.nC_LIO_LIThe tendency to follow the others gaze competes with the attractional binding of the conspecifics facenC_LI

Journal ArticleDOI
TL;DR: This article presents a novel approach to the study of primate personality and illustrates it with a study of capuchin monkeys, using both statistical and non-statistical methods to analyse data from behavioural observations of a group of capuchins in captivity.
Abstract: This article presents a novel approach to the study of primate personality and illustrates it with a study of capuchin monkeys. While most personality studies with capuchin monkeys have used rating questionnaires, the research method of this study relies instead on direct behaviour observations. In an effort to capitalize on the full richness of behavioural observation data, we used both statistical and non-statistical methods to analyse data from behavioural observations of a group of capuchin monkeys in captivity. Interest in capuchin monkeys as a species has increased due to their cognitive capacities, behavioural flexibility and complex social structure, as well as many similarities with great apes in dimensions of personality. In this study we focus in three aspects of personality: diversity, flexibility and complexity. Our results provide a detailed picture of these aspects of capuchins’ personality, including the degree of “predictability” and “unusualness” of individual capuchins’ behaviour.

Journal ArticleDOI
TL;DR: The data obtained indicate a wide circulation of HAV among monkeys born in the Adler Primate Center and among the imported animals, andMarkers of “fresh” HAV infection varied depending on the species of monkeys and their origin.
Abstract: Hepatitis A is a widespread viral infection. The HAV strains of “human” and “monkey” origin are similar in their morphological and antigenic properties, but differ genotypically. The aim of this research was a comparative study of serological and molecular-genetic markers of HAV infection in monkeys born at the Adler Primate Center and in those imported from different countries. Material and methods. Fecal samples ( n = 313) and serum ( n = 266) from various species of monkey using ELISA and RT-PCR were studied. Results and discussion. The frequency of anti-HAV-IgG was high (78.9%) in imported animals (vervet monkeys from Tanzania and cynomolgus monkeys from Vietnam) and as well as in various species of monkeys (rhesus monkeys, cynomolgus monkeys, green monkeys and papio hamadryas) of the Center (88.6%). At the same time, in the imported monkeys, the markers of “fresh” HAV infection (IgM-27.2%, Ag-HAV-16.7%, RNA-22.0%) were detected significantly more often (p> 0.05) than in monkeys kept at the Colony (IgM-7.5%, HAV-Ag – 5.2%, RNA – 3.6%). In general, anti-IgG reactivity ranged from 1.064 to 2.073 OD 450 , anti-IgM ranged from 0.546 to 1.059 OD 450 . The number of HAV-Ag was 0.496 – 1.995 OD 450 . RNA HAV only in rhesus monkeys and cynomolgys monkeys born at the Colony, as well as in imported vervet monkeys was detected. Conclusions. The data obtained indicate a wide circulation of HAV among monkeys born in the Adler Primate Center and among the imported animals. Markers of “fresh” HAV infection varied depending on the species of monkeys and their origin.

BookDOI
07 Jun 2019
TL;DR: Functional Affinities of Man, Monkeys and Apes as discussed by the authors is a taxonomic and phylogenetic survey and the findings of diverse experimental investigations of lemurs, monkeys, and apes.
Abstract: Originally published in 1933 Functional Affinities of Man, Monkeys and Apes gives a taxonomic and phylogenetic survey and the findings of diverse experimental investigations of lemurs, monkeys, and apes. The book discusses the inter-relationships of different Primates and emphasizes seldom-used approaches to the question of primate phylogeny. The book attempts to show how little they have been systematically tried, and argues for a regard to the proper place of functional investigations in the study of the classification and evolution of Primates. This book will be of interest to anthropologists, scientists and historians alike.

Dissertation
02 May 2019
TL;DR: This article examined the variations of nonhuman primate (NHP) pelage coloration and patterning and found that smaller home-range sizes and dispersal of both sexes may have played a role in the evolution of dichromatic pelage in NHPs.
Abstract: There is a large body of research describing the evolutionary importance of plumage coloration among avian species. However , similar datasets are lacking for mammalian pelage. Furthermore , very little research has examined the variations of nonhuman primate (NHP) pelage coloration and patterning. Primatologists have noted conspicuous differences in coloration and patterning among NHPs , including neo-natal coats and sexual dichromatism. Sexual dichromatism refers to the differences in pelage coloration between the sexes of a single species. Sexual dichromatism is rare , but found among some species of lemurs , New World monkeys , and lesser apes. To illuminate the genetic mechanism of NHP sexual dichromatism , I examined published amino acid sequences for the MC1R and OCA2 genes of nine NHP species across multiple genera. This dataset incorporated sexually dichromatic NHPs including white-cheeked gibbons (Nomascus leucogenys) , lar gibbons (Hylobates lar) , and black howler monkeys (Alouatta caraya). I also examined closely allied monochromatic NHPs including brown lemurs (Eulemur fulvus) , long-tailed macaques (Macaca fascicularis) , black snub-nosed monkeys (Rhinopithecus bieti) , Mueller's gibbon (Hylobates muelleri) , mantled howler monkeys (Alouatta palliata) , and chimpanzees (Pan troglodytes). Comparisons across these species suggest the MC1R gene does not play an important role in pelage coloration. In contrast , the OCA2 sequence of N. leucogenys differed , on average , ~16% from the three monochromatic species. Furthermore , the OCA2 sequences exhibit a low phylogenetic signal , suggesting that this gene may regulate dichromatic pelage. To expand these genetic datasets , I analyzed socioecological variables among these species and found that smaller home-range sizes and dispersal of both sexes may have played a role in the evolution of dichromatic pelage in NHPs.

Journal ArticleDOI
TL;DR: Object exploration and behavioral flexibility in a single group of samango monkeys in an environment in which individuals forage in both gardens and natural forest indicate that Samango monkeys exhibited a spatially complex response to novel objects, and exploration diversity decreased significantly in anthropogenic environments, even as persistence remained largely static across contexts.
Abstract: Research suggests that wild animals in urban areas exhibit heightened behavioral flexibility when they encounter novel human-made objects, but most such studies compared responses in urban populations with those from disjunct populations in less disturbed environments. We therefore know little about intrapopulation variation in cognitive or behavioral flexibility under different conditions of anthropogenic exposure. Here, we investigate object exploration and behavioral flexibility in a single group of samango monkeys (Cercopithecus mitis) in an environment in which individuals forage in both gardens and natural forest. Over 2 months, we presented monkeys with novel, human-made objects in both natural and disturbed areas, varying the position of objects in trees to represent exposed or safer foraging zones. We video-recorded and analyzed interactions with these novel objects, assessing interaction times (an indicator of persistence), exploratory diversity (or motor diversity), and the occurrence of foraging innovations. Results from 67 interactions (29 in natural habitats and 38 in disturbed) indicate that samango monkeys exhibited a spatially complex response to novel objects: in contrast to that in other species, exploration diversity decreased significantly in anthropogenic environments, even as persistence remained largely static across contexts. Monkeys also exhibited foraging innovations by pulling on strings to bring objects closer. This may reduce exposure to danger, as string-pulling was most prevalent in the highest risk condition (ground level in human gardens). Significant intrapopulation variation in behavioral flexibility suggests that samango monkeys adjust the expression of problem-solving behaviors in relation to the degree of human disturbance in their immediate environment.

01 Jan 2019
TL;DR: This chapter is intended to provide a history of the city and its people, as well as some of the characters and situations that have occurred in the city over the years.
Abstract: ..................................................................................................... xii Chapter