Capuchin Monkeys Research Articles

Experimental evidence of parasite-induced behavioural alterations modulated by food availability in wild capuchin monkeys

In disease dynamics, host behaviour can both determine the quantity of parasites a host is exposed to, and be a consequence of infection. Observational and experimental studies in non-human primates have consistently found that parasitic infections result in less movement and reduced foraging, which was interpreted as an adaptive response of the host to counter infection. Variation in host nutritional condition may add complexity to the infection-behaviour relationship, and its influence may shed light on its significance. To experimentally evaluate how host activity and social relationships are affected by the interaction of parasitism and nutrition, during two years we manipulated food availability by provisioning bananas, and helminth infections by applying antiparasitic drugs, in two groups of wild black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. We collected faecal samples to determine the intensity of helminthic infections, as well as data on behaviour and social proximity. Individuals with unmanipulated helminth burdens foraged less than dewormed individuals only when food provisioning was low. Resting time was increased when capuchins were highly provisioned, but it did not vary according to the antiparasitic treatment. Proximity associations to other group members were not affected by the antiparasitic treatment. This is the first experimental evidence of a modulating effect of food availability on the influence of helminth infection on activity in wild primates. The findings are more consistent with an impact on host behaviour due to the debilitating effect caused by parasites than with an adaptive response to help fight infections.

Sagittal suture strain in capuchin monkeys (Sapajus and Cebus) during feeding.

Morphological variation in cranial sutures is used to infer aspects of primate feeding behavior, including diet, but strain regimes across sutures are not well documented. Our aim is to test hypotheses about sagittal suture morphology, strain regime, feeding behavior, and muscle activity relationships in robust Sapajus and gracile Cebus capuchin primates. Morphometrics of sinuosity in three regions of the sagittal suture were compared among museum specimens of Sapajus and Cebus, as well as in robust and gracile lab specimens. In vivo strains and bilateral electromyographic (EMG) activity were recorded from these regions in the temporalis muscles of capuchin primates while they fed on mechanically-varying foods. Sapajus and the anterior suture region exhibited greater sinuosity than Cebus and posterior regions. In vivo data reveal minor differences in strain regime between robust and gracile phenotypes but show higher strain magnitudes in the middle suture region and higher tensile strains anteriorly. After gage location, feeding behavior has the most consistent and strongest impact on strain regime in the sagittal suture. Strain in the anterior suture has a high tension to compression ratio compared to the posterior region, especially during forceful biting in the robust Sapajus-like individual. Sagittal suture complexity in robust capuchins likely reflects feeding behaviors associated with mechanically challenging foods. Sutural strain regimes in other anthropoid primates may also be affected by activity in feeding muscles.

Life and death of a disabled wild capuchin monkey infant.

The evolutionary roots of care for injured, ill, and disabled group members remain unclear. The same can be said about care for dying and dead group members. Accumulating case reports in a variety of nonhuman primates can shed light on these origins. Here we provide a detailed account of interactions of a wild capuchin monkey mother and other group members with a disabled infant before and after its death. Limb disability caused the infant to be in unstable positions when carried, which appeared to increase the frequency of body readjustments by the adults and may have contributed to its death. After death, no adults other than the mother made contact with the corpse, but four immatures approached and touched it. The mother foraged only on flies surrounding the corpse while carrying it, stopped several times to set the corpse down on the branches, and let it finally fall as she leapt between trees. The difficulty of carrying disabled and dead individuals up in the trees may help to explain the scarcity of reports in platyrrhines, and suggests that terrestriality and increasing ease of bipedality may have contributed to the evolution of these behaviors in primates.

Monkey overabundance indirectly affects community seed rain via a disruptive interaction with a keystone palm species

In predator-free fragmented remnants of Brazil's Atlantic Forest, capuchin monkeys (Sapajus nigritus) have become an overabundant consumer of palm heart (Euterpe edulis, palmito), negatively impacting the species local abundance. As palmito fruits are keystone resources for many frugivorous animals, the decline in abundance of reproductive plants may reduce food resources for dispersal agents and alter their foraging patterns. Changes in frugivore foraging patterns might translate into changes in zoochorous seed abundance and seed rain richness. Besides, when palmito is a dominant canopy species in lowland forests, population decline may lead to an increase in the amount of light reaching the understory. In our study, we have shown that in areas where predation by capuchin monkeys have eliminated palmito, the abundance and richness of zoochorous seeds in the seed rain are lower compared with areas with lower or no impact of capuchin-monkeys. The abundance of zoochorous seeds in the seed rain is lower in periods of palmito fruiting in areas where the palm occurs. Canopy openness was found to be higher in the area where capuchin-monkey predation of palm heart was higher. We have concluded that the impact of capuchin monkeys on palmito affects seed rain abundance, most likely due to changes in frugivore foraging patterns. In addition, changes in palmito abundance led to changes in the extent of canopy openness in the area of our study. Therefore, monkey predation on a keystone plant may lead to a series of indirect cascading impacts, potentially affecting plant community and forest regeneration dynamics.

Spatial frequency and global-local visual processing in capuchin monkeys (Sapajus spp.) and humans (Homo sapiens).

Two experiments employing an identity matching-to-sample procedure were carried out to clarify the factors affecting global-local visual processing of capuchin monkeys (Sapajus spp.) in comparison with humans. In the first experiment, we assessed the relative ability of the two species to discriminate high, medium, or low spatial frequencies (HSFs, MSFs, or LSFs). Then, in a second experiment, we determined if the use of a procedure designed to induce a bias toward attending given spatial frequencies could produce a top-down or selection-history modulation of global-local visual processing in capuchins and humans. In the first experiment, monkeys discriminated better HSFs. By contrast, humans discriminated better MSFs and LSFs. The second experiment showed an effect of SF processing on global-local processing in both species. However, this effect was confined to local trials only and occurred under different conditions in the two species. In monkeys, it occurred following a bias toward attending HSFs, whereas in humans, it occurred following a bias toward attending LSFs. These results provide new information about the relative sensitivity of humans and capuchins to different spatial frequencies in vision. Moreover, they suggest that global-local visual processing can be modulated in both humans and monkeys by processes that are not confined to attending one or the other level of stimulus structure. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

The development of expertise at cracking palm nuts by wild bearded capuchin monkeys, Sapajus libidinosus

The development of expertise at cracking palm nuts by wild bearded capuchin monkeys, Sapajus libidinosus

DNA integrity and viability of testicular cells from diverse wild species after slow freezing or vitrification.

Cryopreservation of testicular tissues offers new possibilities to protect endangered species, genetically valuable individuals or even the fertility potential of prepubertal individuals who have died unexpectedly. However, the use of this technique still remains a challenge. In this study, slow freezing and vitrification of testicular tissue was investigated to find out which cryopreservation method could better preserve the viability and DNA integrity of testicular germ cells in diverse wild species. Testes were obtained post-mortem from 18 artiodactyls (wild boar, roe deer, dwarf goat, mhor gazelle, European mouflon, African forest buffalo, Malayan tapir, dorcas gazelle, Iberian ibex, gnu, red river hog), 5 primates (colobus monkey, capuchin monkey, mandrill), 8 carnivores (gray wolf, Persian leopard, binturong, European mink, American black bear, suricata), and 2 rodents (Patagonian mara). The testicles belonged to adult individuals and were cut into small pieces and cryopreserved by needle immersed vitrification or uncontrolled slow freezing using a passive cooling device. After warming or thawing, testicular tissues were enzymatically digested and two germ cell types were differentiated based on their morphology: rounded cells (spermatogonia, spermatocytes, and early spermatids) and elongated cells (elongated spermatids and spermatozoa). Cell viability was assessed by SYBR-14/propidium iodide while DNA fragmentation by TUNEL assay with fluorescence microscope. Our preliminary results revealed that our uncontrolled slow freezing method better preserved the viability and DNA integrity of elongated cells than vitrification. Such trend was observed in all species, being significant in artiodactyls, carnivores, and primates. Similarly, the viability and DNA integrity of rounded cells was also better maintained in primates by uncontrolled slow freezing, while in carnivores, vitrification by needle immersion showed better results in this type of cells. In artiodactyls and rodents both techniques preserved the viability of rounded cells in a similar manner, although the DNA integrity of these cells was greater after needle immersed vitrification in artiodactyls. In conclusion, the effectiveness of each cryopreservation method is affected by the phylogenetic diversity between species and cell type.

Architecture of the inferior parietal cortex in capuchin monkey.

We studied the organization of the inferior parietal cortex (IPC) in five capuchin monkey (6 hemispheres) using cytoarchitectonic (Nissl), myeloarchitectonic (Gallyas), and immune-architectonic (SMI-32 monoclonal antibody) techniques. We partitioned the IPC into five distinct areas: PFG, PG, Opt, PFop, and PGop. Since we used parasagittal sections, we were not able to study area PF due to its far lateral position, which yielded slices that were tangential to the pial surface. Areas PFG, PG, and Opt were in the convexity close to the lateral sulcus, while PFop and PGop were positioned more posteriorly, in the opercular region of IPC. Of all the five regions, area Opt was the one most similar to its analogue in the macaque, especially as revealed with SMI-32 staining. Namely, in both primate species area Opt showed a low density of large pyramidal neurons. Additionally, the apical dendrites of these neurons were sparse and vertically orientated, resembling columns. We also found area PG to be similar: both species exhibited cell body layers with a radial arrangement. On the other hand, Nissl staining revealed area PFG to be architectonically different between New and Old-World monkeys: PFG in the capuchin showed a comparatively higher cell density than in macaques, especially in layers II and IV. These results suggest that evolution may have enabled the functional specialization of these brain regions based on behavioral demands of upper limb use. The small differences in the IPC of the two primates may be linked to interspecies variability.

The shape of lipsmacking: socio-emotional regulation in bearded capuchin monkeys (Sapajus libidinosus).

Capuchin monkeys have rich social relationships and from very young ages they participate in complex interactions with members of their group. Lipsmacking behaviour, which involves at least two individuals in socially mediated interactions, may tell about processes that maintain, accentuate or attenuate emotional exchanges in monkeys. Lipsmacking is a facial expression associated with the establishment and maintenance of affiliative interactions, following under the 'emotional regulation' umbrella, which accounts for the ability to manage behavioural responses. We investigated behaviours related to the emitter and to the receiver (infant) of lipsmacking to answer the question of how lipsmacking occurs. In capuchin monkeys, lipsmacking has been previously understood solely as a face-to-face interaction. Our data show that emitters are engaged with infants, looking longer towards their face and seeking eye contact during the display. However, receivers spend most of the time looking away from the emitter and stay in no contact for nearly half of the time. From naturalistic observations of wild infant capuchin monkeys from Brazil we found that lipsmacking is not restricted to mutual gaze, meaning there are other mechanisms in place than previously known. Our results open paths to new insights about the evolution of socio-emotional displays in primates.

Infecção multissistêmica por Dipetalonema spp. em um macaco-prego (Sapajus nigritus)

Abstract The capuchin monkey (Sapajus nigritus) is one of the primates that make up the wild fauna of Rio Grande do Sul. Like other wild animals, primates suffer from infectious diseases transmitted by insects, including filariasis. This report presents the anatomopathological aspects of a multisystemic infection by Dipetalonema spp. in a capuchin monkey, female, adult, of wild origin, rescued along a highway in the north of the state of Rio Grande do Sul by the road policing service and taken for assistance. In the clinical evaluation, nystagmus and involuntary head movements, semi-comatose state, hyperthermia (38.7ºC), hypovolemia, multiple abrasions and deep skin lacerations covering muscle layers were observed. The patient was hospitalized and medicated, but his clinical picture worsened, which resulted in death. At necropsy, the main findings were in the peritoneal cavity, where there was an accumulation of yellowish serous fluid, marked formation of fibrinous adhesions and numerous free nematode parasites in the cavity. Histologically, microfilariae have been observed in the lumen of blood vessels in the lung, liver, heart, kidneys, spleen, small and large intestines, and brain. Peritonitis, pneumonia and bronchiolitis associated with nematodes, liver damage and cerebral microgliosis with satellitosis, neuronophagia and hemorrhagic malacia were also observed. Adult microfilariae and filarids were submitted to morphometric identification and characterized as belonging to the genus Dipetalonema. Thus, it was concluded that this was a case of multisystemic infection by Dipetalonema spp.

Tooling and Construction: From Nut-Cracking and Stone-Tool Making to Bird Nests and Language

The present paper provides an integrative theory of actions and motor programs for skill in tool use, construction, and language. We analyze preconditions for action as well as making their effects (postconditions) explicit, emphasizing the “how” of action details as well as the “what” of motor programs, aided by conceptual analysis of several brain modeling efforts. The theory is exemplified by analysis of the subtractive construction involved in percussive tooling by capuchin monkeys and Oldowan and Acheulean stone tool making by protohumans before turning to the additive construction of hafted tools. A complementary analysis focused on the construction of bird nests explores the notion of “image” and “stage” in construction. We offer a brief comparison with birdsong before arguing for a very different relation between communication and construction in humans. Pantomime lifts manipulation from practical to communicative action in protohumans, and we consider the role of pedagogy before offering hypotheses on the emergence of human language that suggest how language may have evolved from manual skills. We note that language provides an open-ended means for devising innovations in tool use and construction, but reiterate the importance of this framework for diverse future studies in ethology and comparative psychology.

Poliparasitismo em macacos (Sapajus/Cebus nigritus) mantidos em cativeiro na grande Porto Alegre – RS

Monkeys of the Sapajus and Cebus genera are distributed in South America and are often illegally traded and, when apprehended, are taken to zoos. The objective of this work was to verify the occurrence of helminth eggs in the feces of Capuchin monkeys (Sapajus/Cebus nigritus) in captivity, in a zoo in the metropolitan region of Porto Alegre - RS. Fecal samples of 25 animals were collected non-invasively and processed through flotation and sedimentation techniques. In the study, eggs of gastrointestinal helminths were observed in 68% (17/25) of the animals, belonging to the superfamilies Strongyloidea (88,23%); Rhabditoidea (5,88%) and Oxyuroidea (5,88%). New research should be carried out focusing on strategic plans to control parasites in captive animals.

Adrenomedullary responses to non-invasive cortical stimulation in humans

Abstract Introduction: The discovery of cortical adrenomedullary projections in cebus monkeys suggests that similar pathways exist in humans. Notably, the major corticoadrenomedullary projection regions have human equivalents that can be stimulated non-invasively with repetitive transcranial magnetic stimulation (rTMS). If rTMS can be used to selectively modulate adrenomedullary activity, there may be significant therapeutic benefits for stress-, affective-, or neuroimmune-related disorders. Purpose: To assess resting and stress-induced adrenomedullary neuroendocrine responses to continuous (cTBS) and intermittent (iTBS) theta burst TMS in humans. Methods: 39 healthy young adults (14W) were randomly assigned to three counterbalanced sessions of iTBS (n=19) or cTBS (n=20). Stimulation was applied to motor cortical areas that contain the majority of adrenomedullary projections in non-human primates (primary motor cortex trunk region (M1TRUNK) and presupplementary motor area (preSMA)). The M1 leg region (M1LEG) was used as a spatial control. Stimulation locations were determined based on TMS-evoked electromyographic responses in the rectus abdominus (M1TRUNK) and vastus lateralis (M1LEG) or using a combination of fMRI activity and metanalytical structural coordinates (preSMA). All TMS procedures were performed with a 96mm curved double coil and stereotactic navigation. TBS was applied as 600 biphasic TMS pulses at 80% AMT. Corticoadrenomedullary activity and corticospinal excitability (CSE) were assayed before and after TBS, immediately after maximal exercise, and 60min and 90min after TBS based on plasma epinephrine concentrations and median MEP AUC, respectively. Initial analysis of adrenomedullary responses to rTMS were made with a 2 (protocol) x 3 (visit) x 5 (time-point) mixed methods ANOVA. Results and Conclusions: As expected, exercise resulted in a large epinephrine increase (p<0.0001, 8-fold) overall. Ongoing analysis indicates that target-specific changes in adrenomedullary activity are likely, and similar to CSE, may often be paradoxical. Our preliminary results also suggest that adrenomedullary responses to subthreshold rTMS are principally stress inducible. Research Category and Technology and Methods Translational Research: 10. Transcranial Magnetic Stimulation (TMS) Keywords: Adrenal Medulla, Cortex, Sympathetic Nervous System, Non-Invasive Brain Stimulation

First Camera Trap Evidence of Predation of a Black Capuchin Monkey, Sapajus nigritus, by a Cougar, Puma concolor, in the Brazilian Atlantic Forest

First Camera Trap Evidence of Predation of a Black Capuchin Monkey, Sapajus nigritus, by a Cougar, Puma concolor, in the Brazilian Atlantic Forest

Evidence for abstract representations in children but not capuchin monkeys

The use of abstract higher-level knowledge (also called overhypotheses) allows humans to learn quickly from sparse data and make predictions in new situations. Previous research has suggested that humans may be the only species capable of abstract knowledge formation, but this remains controversial. There is also mixed evidence for when this ability emerges over human development. Kemp et al. (2007) proposed a computational model of how overhypotheses could be learned from sparse examples. We provide the first direct test of this model: an ecologically valid paradigm for testing two species, capuchin monkeys (Sapajus spp.) and 4- to 5-year-old human children. We presented participants with sampled evidence from different containers which suggested that all containers held items of uniform type (type condition) or of uniform size (size condition). Subsequently, we presented two new test containers and an example item from each: a small, high-valued item and a large but low-valued item. Participants could then choose from which test container they would like to receive the next sample – the optimal choice was the container that yielded a large item in the size condition or a high-valued item in the type condition. We compared performance to a priori predictions made by models with and without the capacity to learn overhypotheses. Children's choices were consistent with the model predictions and thus suggest an ability for abstract knowledge formation in the preschool years, whereas monkeys performed at chance level.

Primates at the newly established Camaquiri Conservation Initiative, Limon, Costa Rica

&#x0D; &#x0D; &#x0D; In Costa Rica, Geoffroy’s spider monkey (Ateles geoffroyi ornatus) is classified as ‘Endangered’ according to the IUCN Red List of Threatened Species. Given the threats it faces, this spider monkey was included in the most recent ‘Top 25 Endangered Primate Species’ list published by the IUCN (Schwitzer et al. 2019). The newly established Camaquiri Conservation Initiative (CCI) site, located on 200 ha in northeastern Costa Rica in Caribbean lowland rain forest, harbors a population of these monkeys that has yet to be studied. The population size of these primates and the extent to which their habitat may be fragmented is unknown. We conducted transect surveys of spider monkeys, mantled howling monkeys (Alouatta palliata) and Panamanian white-faced capuchins (Cebus imitator) at Camaquiri in 2019, 2020 and 2021 over the course of 13.5 days, covering 32 km total, to establish baseline information important for this new reserve’s conservation management plan, and for providing a rough estimate of the number of study subjects available for potential researchers. We recorded, minimally, 10 different individual spider monkeys in at least one community, at least three different howling monkey groups and at least one capuchin monkey group resident at CCI. Given that large patches of healthy, intact tropical forest are rarely conserved in Central America, Camaquiri provides an opportunity to conserve endangered primate species and to contribute to our knowledge of these animals. Additionally, its proximity to other field stations provides opportunities for studies of patch connectivity, habitat quality and other characteristics that influence primate populations in this region.&#x0D; &#x0D; &#x0D;

Installation and monitoring of a canopy bridge connecting Atlantic Forest fragments containing endangered species in Northeastern Brazil

Abstract In 2019, a canopy bridge was built connecting two fragments of the Atlantic Forest separated by the Pacatuba unpaved road within the Pacatuba-Gargaú Corridor. This bridge was built as part of the Brazilian National Action Plan for the Conservation of Northeastern Primates (Plano de Ação Nacional para Conservação dos Primatas do Nordeste – PAN PRINE). The forest fragments contain a variety of mammal species, including the endangered primate species Alouatta belzebul and Sapajus flavius. Between September 2019 and March 2020, we monitored the canopy bridge continuously with a Bushnell camera trap; for a total of 204 days of sampling, resulting in evidence of 113 independent passage events. During the monitoring period, four mammal species used the canopy bridge, the Endangered Sapajus flavius (blond capuchin monkey), Callithrix jacchus (common marmoset), Marmosa demerarae (woolly mouse opossum), and Marmosa murina (murine mouse opossum). The common marmoset (Callithrix jacchus) used the bridge most frequently, representing 50.44% of the passage events (57), while the blond capuchin monkey (S. flavius) crossed the bridge in 30 events (26.5% of total crossings). All other mammals used the bridge less frequently than the primates (23% of crossings were of opossums). There was no record of crossings by the red-handed howler monkey (Alouatta belzebul) during the monitoring period. The construction of the canopy bridge within the Pacatuba-Gargaú forest corridor promoted structural and functional connectivity of the forest habitats, affecting the movement of the Endangered blond capuchin monkey and the common marmoset and benefiting other arboreal mammal species. The results indicate that monitoring the use of this canopy bridge provided important insights into the behaviour and ecology of the species studied (e.g., activity patterns, social interactions, group sizes, and reproduction, among many others). In addition, the use of the bridge decreases the risks of animal-vehicle collisions and electrocutions. Considering our results, we strongly recommend constructing and implementing canopy bridges as a strategy for the conservation of arboreal species living in fragmented forest areas.

Observation of Masturbation After Visual Sexual Stimuli From Conspecifics in a Captive Male Bearded Capuchin (Sapajus libidinosus).

Masturbation is part of the natural behavioral repertoire of primates, with visual sexual stimuli known to trigger this behavior. Here, we report masturbation events triggered by visual sexual stimulus (VSS) in the South American primate Sapajus libidinosus. We observed a multi-male multi-female captive colony of 17 bearded capuchins between January and October 2014. Over this period, we registered 11 copulation events, 68 attempt copulations, and five masturbation events. The same low-ranking male (named Fu) performed all masturbation events. Fu directly looked at other individuals engaged in sexual displays while he masturbated in three events. The masturbation events associated with VSS lasted up to 2min and 40s. Our observations show that VSS can trigger masturbation in capuchin monkeys. The low hierarchy rank of the male, and the consequent lack of mating opportunities in the multi-male multi-female recently formed group in captivity, may have prompted the masturbation events.

Behaviour of tufted capuchin monkeys in a snowdrift game: is there a role for self-control?

Social dilemmas play an important role in the study of cooperative behaviours. In this experiment we tested the strategies adopted by tufted capuchin monkeys, Sapajus spp., when faced with a cooperative situation involving a conflict of interest, simulating a Snowdrift game. We tested 12 capuchin monkeys (six dyads) in two experimental conditions: Snowdrift (cooperation) and Competition. Monkeys had the opportunity to pull a string to move a rotating bar and obtain a reward while delivering a different reward to their partner. Pulling in the Snowdrift condition delivered a smaller reward to the individual pulling the string and a larger reward to the partner, while the opposite happened in the Competition condition. If neither monkey pulled within 30 s, neither received a reward. Monkeys were also individually tested in a battery of self-control tasks. Capuchin monkeys successfully coordinated (i.e. obtained a reward) in 100% of trials and flexibly adapted their behaviour to the different experimental conditions, by pulling earlier in the Competition and later in the Snowdrift condition. Dominance rank and self-control had no effect on the latencies to pull in either experimental condition. No evidence of any alternation strategy was observed. Our results suggest that capuchin monkeys can solve a conflict of interest without engaging in complex calculations. • Capuchin monkeys faced a cooperative task involving a conflict of interests. • They flexibly adapted to the different experimental conditions. • Their behaviour was not influenced by self-control or dominance rank.

Holocene capuchin-monkey stone tool deposits shed doubts on the human origin of archeological sites from the Pleistocene of Brazil

New World capuchin monkeys are well-known by their ability to solve problems using stone tools that have the characteristics and morphology of some human-made stone tools. The aim of the present contribution is to carry out brief comparisons between the Pleistocene archeological sites from Brazil (e.g. Pedra Furada, Sitio do Meio, Vale da Pedra Furada, Toca da Tira Peia) and capuchin-made stone tool deposits. Pleistocene sites from Brazil are characterized by the exclusive use of immediately available raw material, the predominance of unifacial flaking, and abundance of cortical flakes, together with the absence of blades and bifacial thinning techniques. In all these aspects, the sites resemble capuchin-made lithic deposits and lack a number of human attributes. In sum, based on positive and negative evidence we are confident that the early archeological sites from Brazil may not be human-derived but may belong to capuchin monkeys.