Capuchin Monkeys Research Articles

Primate reintroduction promotes the recruitment of large-seeded plants via secondary dispersal

The loss of larger frugivores alters seed dispersal. Species reintroductions have been proposed as a strategy for reversing local disperser extinctions. However, their effects on ecological processes have seldom been assessed. Howler monkeys (Alouatta guariba) have been reintroduced in Tijuca National Park, a defaunated Atlantic Forest fragment. We compared the fate of seeds dispersed by howlers to dispersal by two other frugivores present in the park: capuchin monkeys (Sapajus nigritus) and guans (Penelope superciliaris). Howlers produce clumped defecations that attract dung beetles, which provide secondary dispersal by burying seeds embedded in feces. We expected that seeds dispersed by howlers would have a different fate from those dispersed by capuchins and guans, since their scattered defecations are less attractive to dung beetles. We followed the fate of seeds 3–14 mm in diameter through three processes after seed deposition: secondary dispersal, predation, and seedling emergence. We estimated the probabilities in each step according to the primary disperser and plant species. Dispersal by howlers increased the recruitment of large-seeded plants because of the higher probability of secondary dispersal of the seeds in their feces. Fewer of the seeds dispersed by capuchins or guans were buried, regardless of size, and burial depths were shallower. For 3 mm seeds, the final recruitment probability was similar across frugivores. However, more of the larger seeds reached the seedling stage when dispersed by howlers since they were buried more deeply, which increased their survival without affecting seedling emergence. Reintroductions can thus contribute to restoring ecological processes.

Urine washing in urban robust capuchin monkeys (Sapajus sp.): The relation with visitors.

In primates, urine washing (UW) is a behavior in which individuals intentionally deposit urine on their bodies. Social and nonsocial hypotheses have been proposed to explain the adaptive function of this behavior. For capuchins, different functions have been assigned for UW, suggesting it as a flexible behavior, but studies have been mainly in captivity. However, no investigations have been performed in urban environments, where these animals can modify their behavior. Our goal was to study UW in a semi-provisioned group of an introduced unknown robust capuchin species (Sapajus sp.) living in a tiny urban fragment in Foz do Iguaçu, Brazil, where they have contact with humans. We assessed the influence of social (sexual, agonistic, and anointing behaviors) and environmental (temperature, relative air humidity, height of the monkeys in the trees, number of people present in the fragment, and human-monkey interactions) variables, the influence of behavior before and after UW, and the influence of sex-age classes, on the frequency of UW. We observed 75 records of UW in 300 h of observations, where urine was mostly deposited on hands and passed on to feet (95%). There were no significant differences in the frequency of the behavior between sex-age classes nor in the behaviors before and after UW. Around 50% of UW took place in the late morning and we found no correlation between UW and temperature, relative air humidity, nor the heights of the monkeys in the trees. However, we found a significant association between UW and the daily number of people in the fragment, but not between UW and human-monkey interactions, anointing, agonisms, and sexual behavior. Our study increases the scope of UW flexibility by identifying the presence of visitors affecting the occurrence of this behavior. We discussed different possibilities through which people could influence the capuchins to display UW.

Haematology, physiological parameters, morphometry and parasitological status of rescued bearded capuchin monkeys (Sapajus libidinosus).

There are few studies on the physiology and haematology of rescued bearded capuchin monkeys. These are necessary to better understand the health and welfare status of the animals, including when performing reintroductions, and to avoid zoonoses. We aimed to obtain physiological and haematological values, morphometry and parasitological status of 26 bearded capuchins in two rescue centres in Northeast Brazil. We found sex- and age-related differences in respiratory rate, body weight and body mass index, but not haematology. The haematological values obtained were significantly different from published data but within the reference intervals for the species. Animals infected with Ancylostoma spp. had significantly lower values in the parameters: haemoglobin concentration, mean corpuscular volume and mean corpuscular haemoglobin concentration than non-infected individuals. Physiological and haematological values of rescued capuchins were similar to those found in previous studies. Ancylostomiasis appears to cause alterations to haematological values of this species.

Changes in the Behavior Pattern of Female Capuchin Monkeys After Chronic Administration of Hormonal Contraceptives

Changes in the Behavior Pattern of Female Capuchin Monkeys After Chronic Administration of Hormonal Contraceptives

Recently Integrated Alu Elements in Capuchin Monkeys: A Resource for Cebus/Sapajus Genomics.

Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus. Further, all tufted capuchins were assigned to a single species, Cebus apella, despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus, with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins (Cebus imitator; [Cebus_imitator_1.0] and Sapajus apella [GSC_monkey_1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. Reported here are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.

A new robust multivariate mode estimator for eye-tracking calibration.

We propose in this work a new method for estimating the main mode of multivariate distributions, with application to eye-tracking calibration. When performing eye-tracking experiments with poorly cooperative subjects, such as infants or monkeys, the calibration data generally suffer from high contamination. Outliers are typically organized in clusters, corresponding to fixations in the time intervals when subjects were not looking at the calibration points. In this type of multimodal distributions, most central tendency measures fail at estimating the principal fixation coordinates (the first mode), resulting in errors and inaccuracies when mapping the gaze to the screen coordinates. Here, we developed a new algorithm to identify the first mode of multivariate distributions, named BRIL, which relies on recursive depth-based filtering. This novel approach was tested on artificial mixtures of Gaussian and Uniform distributions, and compared to existing methods (conventional depth medians, robust estimators of location and scatter, and clustering-based approaches). We obtained outstanding performances, even for distributions containing very high proportions of outliers, both grouped in clusters and randomly distributed. Finally, we demonstrate the strength of our method in a real-world scenario using experimental data from eye-tracking calibrations with Capuchin monkeys, especially for highly contaminated distributions where other algorithms typically lack accuracy.

Population‐level inference for home‐range areas

Abstract Home‐range estimates are a common product of animal tracking data, as each range represents the area needed by a given individual. Population‐level inference of home‐range areas—where multiple individual home ranges are considered to be sampled from a population—is also important to evaluate changes over time, space or covariates such as habitat quality or fragmentation, and for comparative analyses of species averages. Population‐level home‐range parameters have traditionally been estimated by first assuming that the input tracking data were sampled independently when calculating home ranges via conventional kernel density estimation (KDE) or minimal convex polygon (MCP) methods, and then assuming that those individual home ranges were measured exactly when calculating the population‐level estimates. This conventional approach does not account for the temporal autocorrelation that is inherent in modern tracking data, nor for the uncertainties of each individual home‐range estimate, which are often large and heterogeneous. Here, we introduce a statistically and computationally efficient framework for the population‐level analysis of home‐range areas, based on autocorrelated kernel density estimation (AKDE), that can account for variable temporal autocorrelation and estimation uncertainty. We apply our method to empirical examples on lowland tapir Tapirus terrestris, kinkajou Potos flavus, white‐nosed coati Nasua narica, white‐faced capuchin monkey Cebus capucinus and spider monkey Ateles geoffroyi, and quantify differences between species, environments and sexes. Our approach allows researchers to more accurately compare different populations with different movement behaviours or sampling schedules while retaining statistical precision and power when individual home‐range uncertainties vary. Finally, we emphasize the estimation of effect sizes when comparing populations, rather than mere significance tests.

Identification of multiple TAR DNA binding protein retropseudogene lineages during the evolution of primates

The TAR DNA Binding Protein (TARDBP) gene has become relevant after the discovery of its several pathogenic mutations. The lack of evolutionary history is in contrast to the amount of studies found in the literature. This study investigated the evolutionary dynamics associated with the retrotransposition of the TARDBP gene in primates. We identified novel retropseudogenes that likely originated in the ancestors of anthropoids, catarrhines, and lemuriformes, i.e. the strepsirrhine clade that inhabit Madagascar. We also found species-specific retropseudogenes in the Philippine tarsier, Bolivian squirrel monkey, capuchin monkey and vervet. The identification of a retropseudocopy of the TARDBP gene overlapping a lncRNA that is potentially expressed opens a new avenue to investigate TARDBP gene regulation, especially in the context of TARDBP associated pathologies.

Feeding postural behaviors and food geometric and material properties in bearded capuchin monkeys (Sapajus libidinosus)

ObjectivesFoods that are geometrically and mechanically challenging to eat have been associated with specializations in feeding behavior and craniodental morphology across primates, and many of these foods are embedded, requiring a variety of positional behaviors during feeding. However, variation in positional behaviors in response to food properties is not well understood. Here, we examine differences in feeding postural behaviors across feeding events in relation to substrate and food geometric and material properties in a species of extractive foragers, bearded capuchins (Sapajus libidinosus).Methods and materialsWe coded over 1400 co‐occurring postural and feeding behaviors, their durations, and relative sizes of substrate and food from videos recorded at Fazenda Boa Vista in Gilbués, Piauí, Brazil. Food material properties were measured from foods collected at the time of the video recordings.ResultsOur results suggest that bearded capuchin feeding postures significantly differ across the feeding sequence, with substrate size, and between foods of high and low toughness and elastic modulus. Feeding postures were less variable for highly mechanically challenging foods. Food size also had a significant effect on postural behaviors. Large foods were more likely to be associated with suspended postures and small foods with sitting and squatting. Feeding postural behaviors were best explained by a combination of substrate and food variables.ConclusionsOur results indicate that food geometric and mechanical properties have a significant influence on feeding postural behaviors in bearded capuchins. We posit that feeding postural behaviors reflect a combination of substrate variables and food properties, and large, mechanically challenging foods have a limiting effect on postural variation.

First report of Dipetalonema gracile in a captive Marcgrave’s capuchin monkey (Sapajus flavius) in northeastern Brazil: Scientific communication

Parasitic infections are important concern to the Wildlife Conservation Biology, particularly in endangered species. Herein, we report a parasitism by Dipetalonema gracile Rudolphi, 1809 (Spirurida, Filarioidea, Onchocercidae), in the peritoneal cavity of a captive Marcgrave’s capuchin monkey (Sapajus flavius) that died at the Wild Animal Screening Center (CETAS) of the Brazilian Institute for the Environment and Renewable Natural Resources (IBAMA) in the municipality of Cabedelo, state of Paraíba, northeastern Brazil. The necropsy revealed two filarial worms D. gracile in the abdominal cavity. Exudates, thin fibrin layers and fibrous adhesions were also present in the mesentery and spleen capsule. The mesenteric, mandibular, and tracheobronchial lymph nodes were enlarged. Multiple small nodules were seen in the spleen parenchyma. Microscopic examination of the lymph nodes and spleen revealed markedly and diffuse inflammatory reaction, with edema, plasma cells, eosinophils, histiocytes, lymphocytes and rare multinuclear giant cells, with obliteration of the normal histological architecture of the organ. This is the first report of D. gracile parasitism in Marcgrave’s capuchin monkeys, a critically endangered species. Studies of this nature significantly contribute to the knowledge of the parasitic fauna of endangered species, in addition to helping to formulate conservation strategies (in situ and ex situ) and records of new hosts and new areas of occurrence of parasites.

Making sense of monkey business: Re-examining tests of animal rationality

This paper re-examines research that studies economic rationality using experimental data generated by nonhuman animals (e.g. rats, pigeons, monkeys, etc.). The standard experimental methodology to elicit choices from nonhuman animals allows a researcher to test three types of economic rationality: standard deterministic utility maximization, average choice rationality, and random utility maximization. Most of the research has evaluated whether animals satisfy average choice rationality. We describe the difference between these models and check each type of rationality on capuchin monkey data from Chen et al.(2006). We reject standard deterministic utility maximization and random utility maximization for most subjects, but we cannot reject average choice rationality. This paper is the first to provide a statistical test for average choice rationality.

Innovative composite tool use by Goffin\u2019s cockatoos (Cacatua goffiniana)

Composite tool use (using more than one tool simultaneously to achieve an end) has played a significant role in the development of human technology. Typically, it depends on a number of specific and often complex spatial relations and there are thus very few reported cases in non-human animals (e.g., specific nut-cracking techniques in chimpanzees and capuchin monkeys). The innovative strategies underlying the innovation and spread of tool manufacture and associative tool use (using > 1 tools) across tool using animals is an important milestone towards a better understanding of the evolution of human technology. We tested Goffin’s cockatoos on a composite tool problem, the ‘Golf Club Task’, that requires the use of two objects in combination (one used to control the free movement of a second) to get a reward. We demonstrate that these parrots can innovate composite tool use by actively controlling the position of the end effector and movement of both objects involved in a goal directed manner. The consistent use of different techniques by different subjects highlights the innovative nature of the individual solutions. To test whether the solution could be socially transmitted, we conducted a second study, which provided only tentative evidence for emulative learning. To our knowledge, this indicates that the cognitive preconditions for composite tool use have also evolved outside the primate lineage.

Dominance and social interaction patterns in brown capuchin monkey (Cebus [Sapajus] apella) social networks.

Strong, stable social bonds in primates are characterized by high levels of social affiliation, low levels of aggression, minimal stress, and affiliative reciprocity within the dyad. In relatively well-studied catarrhine monkeys, these bonds tend to form most frequently between kin, animals close in age, and animals close in rank. This results in patterns of affiliation in which kin, similarly aged animals, and like-ranked animals tend to affiliate and patterns of aggression and submission where animals tend to aggress more toward nonkin and closely ranked animals, and submit more toward distantly ranked animals. However, literature on how affiliative and agonistic relationships are organized in platyrrhine primate species like brown capuchin monkeys is limited and conflicting. In this study, we used social network analyses to characterize how age, sex, maternal kinship, and dominance rank relate to the patterns of submissive, aggressive, contact, and grooming interactions in a group of captive brown capuchin monkeys. Like catarrhine monkeys, brown capuchin monkeys showed a steep linear dominance hierarchy, tended to affiliate with kin, similarly aged animals, and like-ranked animals, and tended to aggress more toward nonkin. However, our monkeys showed a pattern of affiliation and grooming down the hierarchy that is inconsistent with grooming up the hierarchy patterns often seen in catarrhine monkey groups, suggesting that brown capuchins do not compete for access to higher ranking social partners. Higher ranking monkeys were most central to the aggression network, and lower ranking monkeys were most central to the submission network. Mid-ranking monkeys were the most central to the contact network, suggesting that they may play an important role in the affiliative cohesion of the group. These results inform our understanding of brown capuchin social behavior specifically, and of how demographic factors relate to social organization in platyrrhine primates generally.

Endogenous cortisol correlates with performance under pressure on a working memory task in capuchin monkeys

Humans often experience striking performance deficits when their outcomes are determined by their own performance, colloquially referred to as “choking under pressure.” Physiological stress responses that have been linked to both choking and thriving are well-conserved in primates, but it is unknown whether other primates experience similar effects of pressure. Understanding whether this occurs and, if so, its physiological correlates, will help clarify the evolution and proximate causes of choking in humans. To address this, we trained capuchin monkeys on a computer game that had clearly denoted high- and low-pressure trials, then tested them on trials with the same signals of high pressure, but no difference in task difficulty. Monkeys significantly varied in whether they performed worse or better on high-pressure testing trials and performance improved as monkeys gained experience with performing under pressure. Baseline levels of cortisol were significantly negatively related to performance on high-pressure trials as compared to low-pressure trials. Taken together, this indicates that less experience with pressure may interact with long-term stress to produce choking behavior in early sessions of a task. Our results suggest that performance deficits (or improvements) under pressure are not solely due to human specific factors but are rooted in evolutionarily conserved biological factors.

Detecção molecular e análise filogenética de Trypanosoma spp. em primatas neotropicais do estado do Rio de Janeiro, Brasil

ABSTRACT: Trypanosoma spp. infection is a problem in many tropical countries, infecting several animal species, including humans. The aim of the present study was to identify the Trypanosoma species in Neotropical primates from Rio de Janeiro state and compare the results with other reports both phylogenetically and geographically. Molecular detection was based on the 18 SSU gene. The sequences obtained in the PCR were sequenced and compared with others previously deposited in GenBank. These sequences were used to perform phylogenetic analysis and make a distribution map of primate species infected by Trypanosoma species in Brazil. Among 34 monkeys, five capuchin monkeys (Sapajus spp.) and one marmoset (Callithrix spp.) showed Trypanosoma spp. sequences in the same clade of Trypanosoma minasense and three capuchin monkeys’ sequences were in the same clade of Trypanosoma cruzi. The Atlantic Forest and the Brazilian Amazon are the regions with the highest frequency of studies about Trypanosoma spp. and variety of Neotropical primate hosts. These are areas that deserve attention regarding the conservation of biodiversity, but it also makes evident the lack of studies with Neotropical primates in other regions of the country, as well as multidisciplinary studies to better understand the host pathogen relationships.

Comparative study between ketamine-S-dexmedetomidine and ketamine-S-midazolam-methadone in the anesthesia of capuchin monkeys (Sapajus apella)

ABSTRACT: Anesthetic protocols have been developed to obtain the most effective and safe association in wildlife. This study compared the anesthetic effects and cardiorespiratory parameters of ketamine-S (+) (10 mg/kg)/dexmedetomidine (0.020 mg/kg) (KD ) and ketamine-S (+) (10 mg/kg)/midazolam (0.5 mg/kg)/methadone (1.0 mg/kg) (KMM ) in capuchin monkeys (Sapajus apella). Eight capuchin monkeys were randomly assigned to KD (n = 4) or KMM (n = 4) to evaluate induction, immobilization, and recovery scores, heart and respiratory rate parameters, besides systolic, mean, diastolic arterial pressure and arterial blood gas. There was no difference (P = 0.56) in the quality of induction, immobilization, and anesthetic recovery between the protocols. The time for anesthetic induction was 4 ± 1 min in the KD group and 5 ± 1 min in the KMM group, and these values were statistically equal (P = 0.28). The mean immobilization time in the KD and KMM groups were 35 ± 13 and 33 ± 15 min, respectively. Heart rate was lower in animals in the KD group (P < 0.001), while respiratory rate (P = 0.03), and mean blood pressure (P = 0.046) were higher than that of the animals in the KMM group. Respiratory acidosis occurred in the KMM group, with lower pH (7.25±0.047; P = 0.0055) and higher pCO2 (51 ± 6;mmHg; P = 0.008). Both protocols exhibited good induction quality, immobilization, and anesthetic recovery, despite cardiorespiratory and blood gas alterations observed, which warrants monitoring of cardiorespiratory variables during KD or KMM chemical restraint.

Intra and inter-monkey transmission of bacteria in wild black capuchins monkeys (Sapajus nigritus): a preliminary study.

Intra and inter-monkey transmission of bacteria in wild black capuchins monkeys (Sapajus nigritus): a preliminary study.

Lessons From New South Wales, Queensland, and British Columbia to Assist South Africa in Adequately Regulating the Keeping of Assistance Animals by Disabled Persons in Sectional Title Schemes

South African legislation contains only one subrule in the Sectional Titles Schemes Management Regulations about the keeping of assistance animals in sectional title schemes. This subrule provides that an owner or occupier suffering from a disability who reasonably requires a guide, hearing, or assistance dog must be considered to have the trustees’ consent to keep that animal in a section and to accompany it on the common property. I submit that this subrule falls hopelessly short of regulating this matter adequately and that lessons in this regard can be learned from the comparable Australian jurisdictions of New South Wales and Queensland, and the Canadian jurisdiction of British Columbia. First, this subrule makes no reference to anti-discrimination legislation or legislation dealing with the keeping of dogs which is found in the comparable provisions in the selected jurisdictions. Second, no clear distinction is drawn between service dogs and assistance dogs. It appears that assistance dogs are equated with service dogs which are trained to cater for a specific disability in a disabled person while those suffering from illnesses like depression could also benefit from the mere presence of a dog without any specific training. Third, the rule applies only to assistance dogs while the United States, for example, also provides for miniature horses and Capuchin monkeys to assist persons with disabilities. Fourth, save for guide and hearing dogs, inadequate provision is made for the training of other types of assistance animals. In some cases, disabled persons are allowed to train their own assistance animals without the animal and the disabled person having to comply with strict competency tests, for example, the “public access test” required in Queensland. Finally, there is no agreement regarding what type of disability would qualify for assistance by an assistance animal or what evidence a disabled owner or occupier must provide as proof that he or she reasonably requires an assistance animal.

Knowledge, Attitudes and Practices Regarding Sylvatic Rabies among High-Risk Households in Ceará State, Brazil.

Rabies transmitted by sylvatic populations has become an increasing concern in Brazil. A total of 113 participants with a history of contact with sylvatic populations were interviewed in 27 municipalities of Ceará State in northeast Brazil. Questionnaires included questions on knowledge, attitudes and practices (KAP) regarding sylvatic rabies. Most of the respondents (92%) knew about rabies and confirmed at least one species that transmitted the disease (79.6%). Of these respondents, 69% mentioned monkeys, and 67.2% mentioned dogs. However, 16% of the respondents listed an incorrect species. In general, knowledge on the symptoms and signs and on prevention measures was weak. The majority raised pets (93.8%), most commonly dogs and cats, and, of all the pets, 85.7% were claimed to be vaccinated against rabies. A total of 67.3% reported the appearance of free-living wild animals around their houses, mostly marmosets and wild canids; 18.3% reported that sylvatic populations had attacked animals or humans. Seventy-three percent had raised or still were raising wild animals as pets, mostly capuchin monkeys (79.5%) and marmosets (24.1%). This is the first KAP study on sylvatic rabies in Brazil. The data indicate important knowledge gaps and risk behavior within a high-risk population. There is a need for strengthening and improving sylvatic rabies surveillance and control, combined with the intensification of education and information campaigns.

Observer effects in a remote population of large-headed capuchins, Sapajus macrocephalus

Human observers often are present when researchers record animal behavior, which can create observer effects. These effects are rarely explicitly investigated, often due to the assumption that the study animal is habituated to or unaffected by a human’s presence. We investigated the effect of human pressure gradients on a remote population of large-headed capuchins, Sapajus macrocephalus, looking specifically at the effects of number of observers, distance to observers, and distance to the research base. We conducted this study over 4 months in the Pacaya-Samiria Nature Reserve, Peru, and collected 199 two-minute focal samples of capuchin behavior. We found that capuchin monkeys fed less when human observers were closer to the focal individual, when more observers were present, and when capuchins were closer to the research base. We found no other consistent differences in capuchin monkey behavior across the measured human pressure gradients, although capuchins directed a high proportion of their vigilance toward humans (29% in adults and 47% in infants). Our results support the hypothesis that human pressure gradients influence animal behavior. Given the proportion of human directed vigilance, we recommend that all studies that use human observers to record animal behavior consider human-directed vigilance, record the number of observers, as well as the observer-focal animal distance, to check for these effects.