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Showing papers on "Primate published in 2021"


Journal ArticleDOI
02 Feb 2021-PLOS ONE
TL;DR: In this article, a comparative evaluation of COVID-19 in African green monkeys, rhesus macaques, and cynomolgus macaque following airborne exposure to SARS-CoV-2 was performed to determine critical disease parameters associated with disease progression.
Abstract: Airborne transmission is predicted to be a prevalent route of human exposure with SARS-CoV-2 Aside from African green monkeys, nonhuman primate models that replicate airborne transmission of SARS-CoV-2 have not been investigated A comparative evaluation of COVID-19 in African green monkeys, rhesus macaques, and cynomolgus macaques following airborne exposure to SARS-CoV-2 was performed to determine critical disease parameters associated with disease progression, and establish correlations between primate and human COVID-19 Respiratory abnormalities and viral shedding were noted for all animals, indicating successful infection Cynomolgus macaques developed fever, and thrombocytopenia was measured for African green monkeys and rhesus macaques Type II pneumocyte hyperplasia and alveolar fibrosis were more frequently observed in lung tissue from cynomolgus macaques and African green monkeys The data indicate that, in addition to African green monkeys, macaques can be successfully infected by airborne SARS-CoV-2, providing viable macaque natural transmission models for medical countermeasure evaluation

42 citations


Journal ArticleDOI
02 Nov 2021-Neuron
TL;DR: The PRIMatE Data and Resource Exchange community recently developed a collaboration-based strategic plan to advance nonhuman primate imaging as an integrative approach for multiscale neuroscience as discussed by the authors.

16 citations


Journal ArticleDOI
31 Mar 2021-eLife
TL;DR: Sliwa et al. as mentioned in this paper used functional magnetic resonance imaging (fMRI) acquired at 9.4 Tesla to map the brain areas activated by social interaction observation in awake marmosets.
Abstract: A crucial component of social cognition is to observe and understand the social interactions of other individuals. A promising nonhuman primate model for investigating the neural basis of social interaction observation is the common marmoset (Callithrix jacchus), a small New World primate that shares a rich social repertoire with humans. Here we used functional magnetic resonance imaging (fMRI) acquired at 9.4 Tesla to map the brain areas activated by social interaction observation in awake marmosets. We discovered a network of subcortical and cortical areas, predominately in the anterior lateral frontal and medial frontal cortex, that was specifically activated by social interaction observation. This network resembled that recently identified in Old World macaque monkeys (Sliwa and Freiwald, 2017). Our findings suggest that this network is largely conserved between New and Old World primates and support the use of marmosets for studying the neural basis of social cognition.

15 citations


Journal ArticleDOI
TL;DR: In this paper, the authors investigated the causal role of the anterior cingulate cortex (ACC) in affective responding to threat in rhesus monkeys (Macaca mulatta).
Abstract: Despite many observations of anterior cingulate cortex (ACC) activity related to cognition and affect in humans and nonhuman animals, little is known about the causal role of the ACC in psychological processes. Here, we investigate the ACC’s causal role in affective responding to threat in rhesus monkeys (Macaca mulatta), a species with an ACC largely homologous to humans in structure and connectivity. Male adult monkeys received bilateral ibotenate axon-sparing lesions to the ACC (sulcus and gyrus of areas 24, 32, and 25) and were tested in two classic tasks of monkey threat processing, the human intruder and object responsiveness tasks. Monkeys with ACC lesions did not significantly differ from controls in their overall mean reactivity towards threatening or novel stimuli. However, while control monkeys maintained their reactivity across test days, monkeys with ACC lesions reduced their reactivity towards stimuli as days advanced. Critically, this attenuated reactivity was found even when the stimuli presented each day were novel, suggesting that ACC lesions did not simply cause accelerated adaptation to stimuli as they became less novel over repeated presentations. Rather, these results imply that the primate ACC is necessary for maintaining appropriate affective responses towards potentially harmful and/or novel stimuli. These findings therefore have implications for mood disorders in which responding to threat and novelty is disrupted. Significance statement: Decades of research in humans and nonhuman animals have investigated the role of the anterior cingulate cortex in a huge number and variety of psychological processes spanning cognition and affect, as well as in psychological and neurological diseases. The structure is broadly implicated in psychological processes and mental and neurological health, yet its causal role in these processes has largely gone untested, particularly in primates. Here we demonstrate that when anterior cingulate cortex is completely eliminated, rhesus monkeys are initially responsive to threats, but these responses attenuate rather than persist, resembling a pattern of behavior commonly seen in patients diagnosed with mood disorders.

14 citations


Journal ArticleDOI
04 Nov 2021-Neuron
TL;DR: In this paper, the cortical connectome of the lateral prefrontal cortex (LPFC) was densely mapped using electrical microstimulation combined with functional MRI (EM-fMRI) to find isomorphic mappings between LPFC and five major processing domains composing most of the cerebral cortex.

13 citations


Journal ArticleDOI
TL;DR: It was shown that acute manipulation of disease-causing genes via in vivo gene editing directly led to behavioral changes in adolescent primates, paving the way for the rapid generation of genetically engineered non-human primate models for neurobiological studies and therapeutic development.
Abstract: Although CRISPR/Cas9-mediated gene editing is widely applied to mimic human disorders, whether acute manipulation of disease-causing genes in the brain leads to behavioral abnormalities in non-human primates remains to be determined. Here we induced genetic mutations in MECP2, a critical gene linked to Rett syndrome (RTT) and autism spectrum disorders (ASD), in the hippocampus (DG and CA1–4) of adolescent rhesus monkeys (Macaca mulatta) in vivo via adeno-associated virus (AAV)-delivered Staphylococcus aureus Cas9 with small guide RNAs (sgRNAs) targeting MECP2. In comparison to monkeys injected with AAV-SaCas9 alone (n = 4), numerous autistic-like behavioral abnormalities were identified in the AAV-SaCas9-sgMECP2-injected monkeys (n = 7), including social interaction deficits, abnormal sleep patterns, insensitivity to aversive stimuli, abnormal hand motions, and defective social reward behaviors. Furthermore, some aspects of ASD and RTT, such as stereotypic behaviors, did not appear in the MECP2 gene-edited monkeys, suggesting that different brain areas likely contribute to distinct ASD symptoms. This study showed that acute manipulation of disease-causing genes via in vivo gene editing directly led to behavioral changes in adolescent primates, paving the way for the rapid generation of genetically engineered non-human primate models for neurobiological studies and therapeutic development.

11 citations


Journal ArticleDOI
TL;DR: In this article, the authors evaluated the seasonality in activity budget, diet, and ranging behavior of two groups of Endangered Coimbra-Filho's titi monkeys (Callicebus coimbrai).
Abstract: There is wide variability in primate behavior and ecology Understanding how frugivorous primates behave under different habitat fragmentation levels is key for effective conservation and management of species and their habitats We evaluated the seasonality in activity budget, diet, and ranging behavior of two groups of Endangered Coimbra-Filho's titi monkeys (Callicebus coimbrai) One group inhabited a 14-ha forest fragment, whereas the other lived in a 522-ha fragment We measured the monthly density of trees and lianas available as food sources over 8 months We also collected behavioral and group location data every 5 min, from dawn to dusk, using the scan sampling method The two forest fragments differed seasonally in the number of fruiting food-resource available In the 14-ha fragment, we found that the time spent by titi monkeys feeding, foraging, resting, and traveling differed seasonally In the 522-ha fragment, titi monkeys exhibited seasonal differences in time spent sleeping, socializing, foraging, and revisiting food sources In both titi monkey groups, diets varied seasonally Our findings indicate that Coimbra-Filho's titi monkeys can exhibit behavioral flexibility in their activity budgets, diets, and movement patterns Such flexibility is important for this species to survive in fragmented habitats and may be linked to three key factors: species-specific resource availability, plant species diversity, and the vegetation structure of each forest fragment

9 citations


Journal ArticleDOI
TL;DR: The hypothesis that the connectivity of the prefrontal-parietal regions became relatively elaborated in the simian lineage after divergence from the prosimian lineage is supported.
Abstract: Comparative neuroimaging has been used to identify changes in white matter architecture across primate species phylogenetically close to humans, but few have compared the phylogenetically distant species. Here, we acquired postmortem diffusion imaging data from ring-tailed lemurs (Lemur catta), black-capped squirrel monkeys (Saimiri boliviensis), and rhesus macaques (Macaca mulatta). We were able to establish templates and surfaces allowing us to investigate sulcal, cortical, and white matter anatomy. The results demonstrate an expansion of the frontal projections of the superior longitudinal fasciculus complex in squirrel monkeys and rhesus macaques compared to ring-tailed lemurs, which correlates with sulcal anatomy and the lemur's smaller prefrontal granular cortex. The connectivity of the ventral pathway in the parietal region is also comparatively reduced in ring-tailed lemurs, with the posterior projections of the inferior longitudinal fasciculus not extending toward parietal cortical areas as in the other species. In the squirrel monkeys we note a very specific occipito-parietal anatomy that is apparent in their surface anatomy and the expansion of the posterior projections of the optical radiation. Our study supports the hypothesis that the connectivity of the prefrontal-parietal regions became relatively elaborated in the simian lineage after divergence from the prosimian lineage.

8 citations


Journal ArticleDOI
TL;DR: This article used home-cage training to train two macaque monkeys in a non-match-to-goal task, where each trial required a switch from the choice made in the previous trial to obtain a reward.
Abstract: In neurophysiology, nonhuman primates represent an important model for studying the brain. Typically, monkeys are moved from their home cage to an experimental room daily, where they sit in a primate chair and interact with electronic devices. Refining this procedure would make the researchers’ work easier and improve the animals’ welfare. To address this issue, we used home-cage training to train two macaque monkeys in a non-match-to-goal task, where each trial required a switch from the choice made in the previous trial to obtain a reward. The monkeys were tested in two versions of the task, one in which they acted as the agent in every trial and one in which some trials were completed by a “ghost agent”. We evaluated their involvement in terms of their performance and their interaction with the apparatus. Both monkeys were able to maintain a constant involvement in the task with good, stable performance within sessions in both versions of the task. Our study confirms the feasibility of home-cage training and demonstrates that even with challenging tasks, monkeys can complete a large number of trials at a high performance level, which is a prerequisite for electrophysiological studies of monkey behavior.

8 citations


Journal ArticleDOI
TL;DR: Examination of the frequency of spontaneous urogenital lesions occurring over a 30-year period at the Yerkes and Southwest National Primate Research Centers found renal lesions were reported more frequently than genital lesions in New World monkeys, and renal tumors were infrequent in all species.
Abstract: Given their genetic and anatomic similarities to humans, nonhuman primates (NHPs) may serve as animal models for urogenital diseases of humans. The purpose of this study was to examine the frequency of spontaneous urogenital lesions occurring over a 30-year period at the Yerkes and Southwest National Primate Research Centers and to compare and contrast lesions occurring in Old World versus New World primates. Lesions occurring in the chimpanzee (Pan troglodytes), baboon (Papio spp.), rhesus macaque (Macaca mulatta), cynomolgus macaque (Macaca fascicularis), pig-tailed macaque (Macaca nemestrina), sooty mangabey (Cercocebus atys), common marmoset (Callithrix jacchus), cotton-top tamarin (Sanguinus oedipus), and squirrel monkey (Saimiri sciureus) are discussed. The most common lesions of the kidney were medullary amyloidosis, renal cysts, renal tubular degeneration, glomerulonephritis or glomerulopathy, nephritis, nephrocalcinosis, pyelonephritis, and hydronephrosis. Specific causes of renal tubular disease included pigmentary nephrosis and tubular lipidosis. Renal tumors, including renal adenoma and carcinoma, lymphoma, and nephroblastoma, were infrequent diagnoses in all species. Endometriosis was the most frequently diagnosed lesion of the female genital tract. Of the animals examined in this study, it was most frequent in Old World primates. Leiomyoma was the most common uterine tumor. Granulosa cell tumor was the most frequently observed neoplasm of the ovaries, followed by teratoma. Of animals included in the study, most ovarian tumors occurred in baboons. Neoplasms of the male reproductive tract included interstitial cell tumor, seminoma, penile squamous cell carcinoma, penile papilloma, and histiocytoma. In New World monkeys, renal lesions were reported more frequently than genital lesions.

7 citations


Journal ArticleDOI
TL;DR: In this paper, the effects of a new scent enrichment program on captive red-ruffed lemurs (Varecia rubra), black howler monkeys (Alouatta caraya), siamangs (Symphalangus syndactylus), lar gibbons (Hylobates lar) and orangutans (Pongo pygmas pygmaeus).
Abstract: Captive breeding is vital for primate conservation, with modern zoos serving a crucial role in breeding populations of threatened species and educating the general public. However, captive populations can experience welfare issues that may also undermine their reproductive success. To enhance the wellbeing of endangered zoo primates, we conducted a study to assess the effects of a new scent enrichment program on captive red-ruffed lemurs (Varecia rubra), black howler monkeys (Alouatta caraya), siamangs (Symphalangus syndactylus), lar gibbons (Hylobates lar) and orangutans (Pongo pygmaeus pygmaeus). We combined behavioral observations and fecal endocrinology analyses to evaluate the effects of a series of essential oils (benzoin, lavender, lemongrass) on five captive troops (N = 19) housed at Dudley Zoo & Castle and Twycross Zoo (UK). We recorded observations of natural species-specific and abnormal stress-related behaviors for 480 h using instantaneous scan sampling. We collected 189 fecal samples and measured the fecal cortisol concentrations using radioimmunoassay. We found a significant effect of the scent enrichment on behaviors, with red-ruffed lemurs and black howler monkeys reducing their social interactions, as well as red-ruffed lemurs and lar gibbons decreasing their stress-related behaviors after they were exposed to the series of essential oils. We also found that red-ruffed lemurs displayed a significant increase in fecal glucocorticoids following exposure to essential oils. Our contradictory findings suggest that the effects of this series of essential oils may change depending on the species-specific social lives and olfactory repertoires of primates. In conclusion, we cannot recommend using these essential oils widely with zoo primates without additional evaluation.

Journal ArticleDOI
TL;DR: In this article, the authors used survival/event time models for latency to look and negative binomial mixed models for duration of looking in coppery titi monkeys (Plecturocebus cupreus).
Abstract: The Snake Detection Theory implicates constricting snakes in the origin of primates, and venomous snakes for differences between catarrhine and platyrrhine primate visual systems. Although many studies using different methods have found very rapid snake detection in catarrhines, including humans, to date no studies have examined how quickly platyrrhine primates can detect snakes. We therefore tested in captive coppery titi monkeys (Plecturocebus cupreus) the latency to detect a small portion of visible snake skin. Because titi monkeys are neophobic, we designed a crossover experiment to compare their latency to look and their duration of looking at a snake skin and synthetic feather of two lengths (2.5 cm and uncovered). To test our predictions that the latency to look would be shorter and the duration of looking would be longer for the snake skin, we used survival/event time models for latency to look and negative binomial mixed models for duration of looking. While titi monkeys looked more quickly and for longer at both the snake skin and feather compared to a control, they also looked more quickly and for longer at larger compared to smaller stimuli. This suggests titi monkeys' neophobia may augment their visual abilities to help them avoid dangerous stimuli.

Journal ArticleDOI
TL;DR: In this paper, the authors describe and compare the diet of the golden monkey (Cercopithecus mitis kandti) in both the Virunga massif and the Gishwati forest.
Abstract: Many primates exhibit behavioral flexibility which allows them to adapt to environmental change and different habitat types. The golden monkey (Cercopithecus mitis kandti) is a little-studied endangered primate subspecies endemic to the Virunga massif and the Gishwati forest in central Africa. In the Virunga massif, golden monkeys are mainly found in the bamboo forest, while in the Gishwati forest they live in mixed tropical montane forest. Here we describe and compare the diet of golden monkeys in both fragments. Over 24 consecutive months from January 2017 we used scan sampling to record feeding and ranging behavior of two Virunga groups and one Gishwati group totaling ca. 240 individuals. We also examined the phenology of bamboo and fruit trees, key seasonal food plant species for the monkeys. Golden monkeys fed on more than 100 plant species. The Virunga groups were mostly folivorous (between 72.8% and 87.16% of the diet) and fed mostly on young bamboo leaves and bamboo shoots, while 48.69% of the diet of the Gishwati group consisted of fruit from 22 different tree and shrub species. Bamboo shoots and fruit are seasonally available foods and were consumed regularly throughout the period when they were available. Despite being the smallest of the three study groups, the Gishwati group had a larger home range area (150.07 ha) compared to both Virunga groups (25.24 and 91.3 ha), likely driven by the differences in availability and distribution of fruit and bamboo in the habitats. Like other blue monkey subspecies, golden monkeys appear to have a flexible dietary strategy enabling them to adjust diet and ranging behavior to local habitats and available food resources. Additional studies and continuing conservation efforts are needed to better understand how variation in feeding and ranging ecology affects reproduction, population growth, and carrying capacity.

Journal ArticleDOI
TL;DR: In this article, the authors review the retinal circuits that endow primate ipRGCs with the cone-opponency capable of encoding the color of the sky and contributing to the wide-ranging effects of short-wavelength light on ip-RGC-mediated nonimage-forming visual function in humans.

Journal ArticleDOI
TL;DR: In this paper, a comprehensive medical record review of monkeys that naturally exhibit differences in sociality and found that low social monkeys are more susceptible to traumatic injuries than high-social monkeys.
Abstract: People with autism spectrum disorder (ASD) exhibit a variety of medical morbidities at significantly higher rates than the general population. Using an established monkey model of naturally occurring low sociality, we investigated whether low-social monkeys show an increased burden of medical morbidities compared to their high-social counterparts. We systematically reviewed the medical records of N = 152 (n = 73 low-social; n = 79 high-social) rhesus macaques (Macaca mulatta) to assess the number of traumatic injury, gastrointestinal, and inflammatory events, as well as the presence of rare medical conditions. Subjects' nonsocial scores, determined by the frequency they were observed in a nonsocial state (i.e., alone), and macaque Social Responsiveness Scale-Revised (mSRS-R) scores were also used to test whether individual differences in social functioning were related to medical morbidity burden. Medical morbidity type significantly differed by group, such that low-social monkeys incurred higher rates of traumatic injury compared to high-social monkeys. Nonsocial scores and mSRS-R scores also significantly and positively predicted traumatic injury rates, indicating that monkeys with the greatest social impairment were most impacted on this health measure. These findings from low-social monkeys are consistent with well-documented evidence that people with ASD incur a greater number of traumatic injuries and receive more peer bullying than their neurotypical peers, and add to growing evidence for the face validity of this primate model. LAY SUMMARY: People with autism exhibit multiple medical problems at higher rates than the general population. We conducted a comprehensive medical record review of monkeys that naturally exhibit differences in sociality and found that low-social monkeys are more susceptible to traumatic injuries than high-social monkeys. These results are consistent with reports that people with autism also incur greater traumatic injury and peer bullying and add to growing evidence for the validity of this monkey model.

Journal ArticleDOI
TL;DR: Genetic evidence of fourteen different visual phenotypes is identified among the five sympatric taxa found in the Yasuní Biosphere Reserve in Ecuador, suggesting that interspecific competition among primates may influence intraspecific frequencies of opsin alleles.
Abstract: A recent focus in community ecology has been on how within-species variability shapes interspecific niche partitioning. Primate color vision offers a rich system in which to explore this issue. Most neotropical primates exhibit intraspecific variation in color vision due to allelic variation at the middle-to-long-wavelength opsin gene on the X chromosome. Studies of opsin polymorphisms have typically sampled primates from different sites, limiting the ability to relate this genetic diversity to niche partitioning. We surveyed genetic variation in color vision of five primate species, belonging to all three families of the primate infraorder Platyrrhini, found in the Yasuni Biosphere Reserve in Ecuador. The frugivorous spider monkeys and woolly monkeys (Ateles belzebuth and Lagothrix lagotricha poeppigii, family Atelidae) each had two opsin alleles, and more than 75% of individuals carried the longest-wavelength (553-556 nm) allele. Among the other species, Saimiri sciureus macrodon (family Cebidae) and Pithecia aequatorialis (family Pitheciidae) had three alleles, while Plecturocebus discolor (family Pitheciidae) had four alleles-the largest number yet identified in a wild population of titi monkeys. For all three non-atelid species, the middle-wavelength (545 nm) allele was the most common. Overall, we identified genetic evidence of fourteen different visual phenotypes-seven types of dichromats and seven trichromats-among the five sympatric taxa. The differences we found suggest that interspecific competition among primates may influence intraspecific frequencies of opsin alleles. The diversity we describe invites detailed study of foraging behavior of different vision phenotypes to learn how they may contribute to niche partitioning.

Journal ArticleDOI
TL;DR: The gray mouse lemur (Microcebus murinus), one of the world's smallest primates, is thought to share a similar ecological niche and many anatomical traits with early euprimates.

Journal ArticleDOI
TL;DR: This paper showed that the amyloid plaque microenvironment is not equivalent between rodent and primate species, and that differences in the impact of AD pathology on local metabolism and inflammation might explain established differences in neurodegeneration and functional decline.
Abstract: Age is a major risk factor for late-onset Alzheimer's disease (AD) but seldom features in laboratory models of the disease. Furthermore, heterogeneity in size and density of AD plaques observed in individuals are not recapitulated in transgenic mouse models, presenting an incomplete picture. We show that the amyloid plaque microenvironment is not equivalent between rodent and primate species, and that differences in the impact of AD pathology on local metabolism and inflammation might explain established differences in neurodegeneration and functional decline. Using brain tissue from transgenic APP/PSEN1 mice, rhesus monkeys with age-related amyloid plaques, and human subjects with confirmed AD, we report altered energetics in the plaque microenvironment. Metabolic features included changes in mitochondrial distribution and enzymatic activity, and changes in redox cofactors NAD(P)H that were shared among species. A greater burden of lipofuscin was detected in the brains from monkeys and humans of advanced age compared to transgenic mice. Local inflammatory signatures indexed by astrogliosis and microglial activation were detected in each species; however, the inflamed zone was considerably larger for monkeys and humans. These data demonstrate the advantage of nonhuman primates in modeling the plaque microenvironment, and provide a new framework to investigate how AD pathology might contribute to functional loss.

Journal ArticleDOI
04 May 2021-Primates
TL;DR: In this paper, the authors describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga, and Atlantic forest, and compare the interaction patterns among sites and different group sizes.
Abstract: Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421 h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species’ body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.

Journal ArticleDOI
TL;DR: The absence of active and consistent polyspecific association is shown and identify avoidance in some species pairs in an Asian primate community is identified.
Abstract: Polyspecific associations, in which individuals of multiple species move together, have not been reported in Asian primates. However, only one study in India has shown this lack of association quantitatively. We collected data on interspecific encounters among 5 species of diurnal primates in Danum Valley by censusing 4 predetermined routes of 9.9 km, covering 1544.3 km, and tracking red leaf monkeys (Presbytis rubicunda) for 423 h over 25 mo. We tested the null hypothesis that the frequency and duration of encounters did not differ from chance levels. During censuses, we detected primates 373 times and found 2 species on the same 100-m segment only 6 times. This frequency was not significantly different from the chance level. While following red leaf monkeys, the frequency of encounters was lower than expected by chance with Mueller’s gibbons (Hylobates muelleri) but higher than expected by chance with Bornean orangutans (Pongo pygmaeus) in the nonfruiting season. Interspecific encounters accounted for 6.4% of tracking time, and the encounter duration was significantly longer than expected by chance for orangutans. Red leaf monkeys did not change their rate or direction of travel on meeting another species. We could not distinguish the association between red leaf monkeys and orangutans in the nonfruiting season from the possibility that the two species were independently attracted to the same place. In conclusion, we show the absence of active and consistent polyspecific association and identify avoidance in some species pairs in an Asian primate community.

Journal ArticleDOI
TL;DR: In this article, the authors used behavioral observation methodologies to evaluate the impact of enclosure expansion on the activity budgets of a group of three eastern black-and-white colobus monkeys, Colobus guereza, housed at the Adelaide Zoo in South Australia.
Abstract: Behavior is one of the most observable and informative indicators of animal welfare. This study used behavioral observation methodologies to evaluate the impact of an enclosure expansion on the activity budgets of a group of three eastern black-and-white colobus monkeys, Colobus guereza, housed at the Adelaide Zoo in South Australia. Instantaneous scan sampling methods were used to record the monkeys' behavior before and after they were given access to new aerial walkways at 2-min intervals between 8:30 a.m. and 4:30 p.m., over a total of 109 h (66 baseline hours, 43 post-expansion hours). Broad state behaviors (e.g., social, moving, resting, interacting, and feeding) were recorded and were used to generate activity budgets. Locomotion, feeding, and social behaviors increased following the addition of the aerial walkways, along with an overall increase in activity, attributed to the larger area and increased complexity of the environment. Results indicate that the addition of aerial walkways was effective for increasing the behavioral repertoire in colobus monkeys, aligning activity budgets more closely with their wild counterparts, and increasing active and affiliative behaviors.

Journal ArticleDOI
TL;DR: The authors found that the expanded circumorbits of male red colobus monkeys evolved in response to intense male-male competition and highlighted the underappreciated role of sexual selection in shaping the primate face.
Abstract: Objectives The function of the browridge in primates is a subject of enduring debate. Early studies argued for a role in resisting masticatory stresses, but recent studies have suggested sexual signaling as a biological role. We tested associations between circumorbital form, diet, oral processing, and social behavior in two species of colobus monkey-the king colobus (Colobus polykomos) and western red or bay colobus (Piliocolobus badius). Materials and methods We quantified circumorbital size and dimorphism in a sample of 98 crania. Controlling for age and facial size, we tested whether variation in circumorbital morphology can be explained by variation in diet, oral processing behavior, masticatory muscle size, and mating system. To contextualize our results, we included a broader sample of facial dimorphism for 67 anthropoid species. Results Greater circumorbital thickness is unrelated to the stresses of food processing. King colobus engages in longer bouts of anterior tooth use, chews more per ingestive event, and processes a tougher diet, yet circumorbital thickness of C. polykomos is reduced compared to P. badius. Differences in circumorbital development do not vary with wear or facial size. Greater sexual dimorphism is present in P. badius; comparisons across anthropoids indicated patterns of circumorbital dimorphism were decoupled from overall size dimorphism. Conclusions The expanded circumorbits of male red colobus monkeys evolved in response to intense male-male competition. This hypothesis is consistent with the pattern across anthropoid primates and highlights the underappreciated role of sexual selection in shaping the primate face.

Journal ArticleDOI
TL;DR: The alarm call system of lesser spot-nosed monkeys, a primate that spends most of its time in mixed-species groups while occupying the lowest and presumably most dangerous part of the forest canopy, is analysed, finding evidence for two acoustically distinct calls but, contrary to other primates in the same habitat, no evidence for predator-specific alarms.
Abstract: Forest monkeys often form semi-permanent mixed-species associations to increase group-size related anti-predator benefits without corresponding increases in resource competition. In this study, we analysed the alarm call system of lesser spot-nosed monkeys, a primate that spends most of its time in mixed-species groups while occupying the lowest and presumably most dangerous part of the forest canopy. In contrast to other primate species, we found no evidence for predator-specific alarm calls. Instead, males gave one general alarm call type (‘kroo’) to three main dangers (i.e., crowned eagles, leopards and falling trees) and a second call type (‘tcha-kow’) as a coordinated response to calls produced in non-predatory contexts (‘boom’) by associated male Campbell’s monkeys. Production of ‘kroo’ calls was also strongly affected by the alarm calling behaviour of male Campbell’s monkeys, suggesting that male lesser spot-nosed monkeys adjust their alarm call production to another species’ vocal behaviour. We discuss different hypotheses for this unusual phenomenon and propose that high predation pressure can lead to reliance on other species vocal behaviour to minimise predation. Predation can lead to the evolution of acoustically distinct, predator-specific alarm calls. However, there are occasional reports of species lacking such abilities, despite diverse predation pressure, suggesting that evolutionary mechanisms are more complex. We conducted field experiments to systematically describe the alarm calling behaviour of lesser spot-nosed monkeys, an arboreal primate living in the lower forest strata where pressure from different predators is high. We found evidence for two acoustically distinct calls but, contrary to other primates in the same habitat, no evidence for predator-specific alarms. Instead, callers produced one alarm call type (‘kroo’) to all predator classes and another call type (‘tcha-kow’) to non-predatory dangers, but only as a response to a specific vocalisation of Campbell’s monkeys (‘boom’). The production of both calls was affected by the calling behaviour of Campbell’s monkeys, suggesting that lesser spot-nosed monkey vocal behaviour is dependent on the antipredator behaviour of other species. Our study advances the theory of interspecies interactions and evolution of alarm calls.

Journal ArticleDOI
TL;DR: In this article, the serum biochemical profile of free-ranging red-handed howler monkeys in a highly disturbed area of the eastern Amazon was determined using 20 biochemical variables, including direct bilirubin, creatinine, and alkaline phosphatase.
Abstract: BACKGROUND The red-handed howler monkey (Alouatta belzebul) is one of 116 imperiled Brazilian primate species. We aimed to determine the serum biochemical profile of free-ranging red-handed howler monkeys in a highly disturbed area of the eastern Amazon. METHODS We obtained serum samples from 26 monkeys, in which we analyzed 20 biochemical variables. RESULTS AND CONCLUSIONS Calcium concentration was significantly lower in adult males (1.82 ± 0.25 mmol/L) than in adult females (2.10 ± 0.50 mmol/L). Both adults (males = 89 ± 85 UI/L, females = 62 ± 23 UI/L) had lower alkaline phosphatase serum activity than juvenile females (178 ± 120 UI/L). Adult male had higher levels of the direct bilirubin (13.9 ± 8.2 µmol/L) and creatinine (74.3 ± 19.4 µmol/L) than juvenile females (5.1 ± 1.4 µmol/L and 38.9 ± 15.0 µmol/L, respectively). This detailed biochemical profile may be useful for the management of red-handed howler monkeys in the wild and to support further studies at ex situ facilities.

Journal ArticleDOI
TL;DR: This article found that varicose projection astrocytes are exclusively found in hominoid brains while being absent from other primate brains, and the evolutionary pattern of different types of varicosities-containing processes across animal species remains unresolved.



Journal ArticleDOI
15 Jul 2021
TL;DR: Convergence between results from other taxa supports the hypothesis that the biological mechanisms that allow for primate sociality are shared among species.
Abstract: There is growing evidence that non-human primate sociality is linked to proximate neuroendocrine mechanisms. Arginine vasopressin, endorphins, and oxytocin may be involved in such mechanisms. Here, we perform a preliminary analysis of the social correlates of variation in urinary oxytocin concentrations in mantled howler monkeys (Alouatta palliata). From January to December 2017, we studied 13 adult mantled howler monkeys belonging to two groups. We recorded the occurrence of social interactions (547.5 observation hours); assessed proximity among group members (2,194 instantaneous recordings); and collected 172 urine samples. Urine samples were assayed (ELISA) for oxytocin concentrations, which were corrected for specific gravity, resulting in 54 analyzed samples. Hormone concentrations increased by approximately 62% when individuals were involved in affiliative interactions. With respect to when no affiliative interactions occurred, urinary oxytocin concentrations were higher when dyads with a low-quality social relationship affiliated. These results agree with previous contentions that this hormone is linked to participation in affiliative interactions. Convergence between these and results from other taxa supports the hypothesis that the biological mechanisms that allow for primate sociality are shared among species.

Journal ArticleDOI
TL;DR: Data suggest that depictions of nonhuman primates are implicitly influenced by phylogenetic proximity: the more closely related the primate, the more likely the authors are to depict them as they do ourselves, showing the left cheek.
Abstract: Portraits of humans favour the left cheek, with emotion thought to drive this posing asymmetry. In primates the emotion-dominant right hemisphere predominantly controls the left hemiface, rendering the left cheek anatomically more expressive than the right. As perceptions of nonhuman primates vary with genetic relatedness, depictions of nonhuman primates should theoretically be influenced by their phylogenetic proximity to humans. The present study thus examined whether humans depict nonhuman primates showing the left cheek, and whether depictions vary with evolutionary distance. Photographs of nonhuman primates were sourced from Instagram's "Most recent" feed: great apes (#chimpanzee, #bonobo, #gorilla, #orangutan), lesser apes (#gibbon), Old World monkeys (#baboon, #macaque, #proboscismonkey), New World monkeys (#spidermonkey, #marmosetmonkey, #capuchin), and prosimians (#lemur, #slowloris, #tarsier). The first 500 single-subject images for each hashtag (except #slowloris for which 318 images were available) were coded for pose orientation (left, right) and portrait type (head/torso, full body). As anticipated, there was a left cheek bias for great apes but no bias for more distantly related primates. These data thus suggest that depictions of nonhuman primates are implicitly influenced by phylogenetic proximity: the more closely related the primate, the more likely we are to depict them as we do ourselves, showing the left cheek.

Journal ArticleDOI
TL;DR: In this article, the brain networks underlying vocal production in non-human primates show striking similarities with the human speech production network, and the extent to which the primate vocal cortical network model generalizes to other non-primate mammals remains unclear.