Cebus Apella Research Articles

Parvalbumin expression and distribution in the hippocampal formation of Cebus apella.

New World primates play an important role in biomedical research. However, the literature still lacks information on many structural features of the brain in these species, particularly structures of the hippocampal formation that are related to long-term memory storage. This study was designed to provide information, for the first time, about the distribution and number of neurons expressing parvalbumin-immunoreactivity (PV-I) in the subregions of the hippocampal formation in Cebus apella, a New World primate species commonly used in biomedical research. Our results revealed that for several morphometric variables, PV-I cells differ significantly among the subregions CA1, CA2, CA3, and the hilus. Based upon our findings and those of other studies, we hypothesize that the proportional increase from monkeys to humans in PV-I cell density within CA1 is a factor contributing to the evolution of increased memory formation and storage.

Capuchin monkeys do not show human-like pricing effects.

Recent work in judgment and decision-making has shown that a good's price can have irrational effects on people's preferences. People tend to prefer goods that cost more money and assume that such expensive goods will be more effective, even in cases where the price of the good is itself arbitrary. Although much work has documented the existence of these pricing effects, unfortunately little work has addressed where these price effects come from in the first place. Here we use a comparative approach to distinguish between different accounts of this bias and to explore the origins of these effects. Specifically, we test whether brown capuchin monkeys (Cebus apella) are also susceptible to pricing effects within the context of an experimentally trained token economy. Using a capuchin population previously trained in a token market, we explored whether monkeys used price as an indicator of value across four experiments. Although monkeys demonstrated an understanding of which goods had which prices (consistently shifting preferences to cheaper goods when prices were increased), we observed no evidence that such price information affected their valuation of different kinds of goods. These results suggest that human pricing effects may involve more sophisticated human-unique cognitive capacities, such as an understanding of market forces and signaling.

RECONSTRUCTING THE DIET AND PALEOECOLOGY OF PLIO-PLEISTOCENE CERCOPITHECOIDES WILLIAMSI FROM STERKFONTEIN, SOUTH AFRICA

ABSTRACT The Plio-Pleistocene cave site of Sterkfontein has yielded the remains of Cercopithecoides williamsi, a colobine monkey reconstructed as a terrestrial folivore given its dental morphology, heavily worn teeth and robustly built postcranial skeleton. To address the validity of these dietary and habitat inferences, patterns of dental microwear obtained from low-magnification stereomicroscopy for C. williamsi specimens from Sterkfontein Member 4 (n = 13) are compared to a broad comparative sample of extant primates, including Cebus apella (n = 10), Colobus polykomos, (n = 6), Papio anubis (n = 13), and Papio ursinus (n = 39) as well as extinct Parapapio broomi (n = 12) from Sterkfontein Member 4 and Theropithecus oswaldi danieli (n = 6) from Swartkrans Member 1. Cercopithecoides williamsi exhibits numerous large pits and puncture pits, and few fine scratches. When diet is considered, C. williamsi is closely associated with C. polykomos and C. apella, suggesting folivorous resources and ...

Mitigación de daños provocados por fauna silvestre en cultivos agrícolas en un bosque montano de Bolivia

Wildlife is often blamed for causing damage to human activities, including agricultural practices and the result may be a conflict between human interests and species conservation. A formal assessment of the magnitude of damage is necessary to adequately conduct management practices and an assessment of the efficiency of different management practices is necessary to enable managers to mitigate the conflict with rural people. This study was carried out to evaluate the effectiveness of agricultural management practices and controlled hunting in reducing damage to subsistence annual crops at the Cotapata National Park and Natural Area of Integrated Management. The design included seven fields with modified agricultural practices, four fields subjected to control hunting, and five fields held as controls. We registered cultivar type, density, frequency of visiting species to the field, crops lost to wildlife, species responsible for damage, and crop biomass. Most frequent species in the fields were Dasyprocta punctata and Dasypus novemcinctus. Hunted plots were visited 1.6 times more frequently than agriculturally managed plots. Crop lost to wildlife averaged 7.28% at agriculturally managed plots, 4.59% in plots subjected to hunting, and 27.61% in control plots. Species mainly responsible for damage were Pecari tajacu, D. punctata, and Sapajus apella. We concluded that both management strategies were effective to reduce damage by >50% as compared to unmanaged crop plots.

Visuospatial learning and memory in the Cebus apella and microglial morphology in the molecular layer of the dentate gyrus and CA1 lacunosum molecular layer

We investigated whether the morphology of microglia in the molecular layer of the dentate gyrus (DG-Mol) or in the lacunosum molecular layer of CA1 (CA1-LMol) was correlated with spatial learning and memory in the capuchin monkey (Cebus apella). Learning and memory was tested in 4 monkeys with visuo-spatial, paired associated learning (PAL) tasks from the Cambridge battery of neuropsychological tests. After testing, monkeys were sacrificed, and hippocampi were sectioned. We specifically immunolabeled microglia with an antibody against the adapter binding, ionized calcium protein. Microglia were selected from the middle and outer thirds of the DG-Mol (n=268) and the CA1-LMol (n=185) for three-dimensional reconstructions created with Neurolucida and Neuroexplorer software. Cluster and discriminant analyses, based on microglial morphometric parameters, identified two major morphological microglia phenotypes (types I and II) found in both the CA1-LMol and DG-Mol of all individuals. Compared to type II, type I microglia were significantly smaller, thinner, more tortuous and ramified, and less complex (lower fractal dimensions). PAL performance was both linearly and non-linearly correlated with type I microglial morphological features from the rostral and caudal DG-Mol, but not with microglia from the CA1-LMol. These differences in microglial morphology and correlations with PAL performance were consistent with previous proposals of hippocampal regional contributions for spatial learning and memory. Our results suggested that at least two morphological microglial phenotypes provided distinct physiological roles to learning-associated activity in the rostral and caudal DG-Mol of the monkey brain.

Hand preference in fast-moving versus slow-moving actions in capuchin, Sapajus spp., and squirrel monkeys, Saimiri sciureus

Among the many hand preference studies on nonhuman primates, several have demonstrated the effect of diverse action demands on the direction and magnitude of hand preference. However, few studies have assessed hand preference in the natural repertoire of motor behaviours in nonhuman primates, especially in actions that differ in velocity. Nevertheless, velocity is involved in the coordination between the upper limb joints and could be related to cerebral hemispheric specialization. Indeed, depending on the velocity, some joints, and so some muscles, are used more than others. The purpose of this study was to quantify hand preference across various natural actions to evaluate how the nature of the action modifies hand preference in capuchin and squirrel monkeys. First, we observed seven female tufted capuchin monkeys during spontaneous foraging, performing fast actions (pounding and capturing fast-moving prey) and slow actions (picking fruit, carrying, tapping and catching slow-moving prey). Second, we observed seven squirrel monkeys performing fast actions (capturing fast-moving prey) and slow actions (picking fruit and catching slow-moving prey) in their enclosure. The results showed that (1) capturing fast-moving prey and pounding were associated with a left-hand preference and (2) slow actions were associated with variable hand preferences. Fast manual actions may elicit consistent hand preference. Given that many nonhuman primates use fast actions to capture prey, this possibility deserves further investigation. If this finding is confirmed, a novel link between motor control processes and hand preference can be pursued.

Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys

Here we examine data from a two-year research on the use of sticks as probes by two groups of wild capuchin monkeys (Sapajus libidinosus) in Serra da Capivara National Park (PI), Brazil. The use of sticks as probes is not usually observed among wild tufted capuchin (Sapajus spp.) populations, having been reported as a customary behavior only in SCNP groups. Probe tools are used to access small prey (insects or lizards) in rock cracks or tree trunks, or honey from wasps’ nests, and also to poke toads and poisonous snakes. Probe use is, so far, the only known case in which wild capuchins modify objects used as tools: branches are trimmed off, and tips, thinned. Tool preparation episodes involved up to four modification steps. Contrary to the stone tools used to crack hard nuts, probe tools don’t present any weight constraint for use by females, but there is nevertheless a strong male bias (97%) in the occurrence of probe tool use. There are also no diet biases that could explain this difference. Although males hunt more often than females, the latter main prey items are lizards, which are also the main targets of probe tool use. One possibility is that females may have fewer social opportunities to learn about probe tools.

Feedforward and feedback connections and their relation to the cytox modules of V2 in Cebus monkeys

To study the circuitry related to the ventral stream of visual information processing and its relation to the cytochrome oxidase (CytOx) modules in visual area V2, we injected anterograde and retrograde cholera toxin subunit B (CTb) tracer into nine sites in area V4 in five Cebus apella monkeys. The injection site locations ranged from 2° to 10° eccentricity in the lower visual field representation of V4. Alternate cortical sections, cut tangentially to the pial surface or in the coronal plane, were stained for CTb immunocytochemistry or for CytOx histochemistry or for Nissl. Our results indicate that the V4-projecting cells and terminal-like labeling were located in interstripes and thin CytOx-rich stripes and avoided the CytOx-rich thick stripes in V2. The feedforward projecting cell bodies in V2 were primarily located in the supragranular layers and sparsely located in the infragranular layers, whereas the feedback projections (i.e., the terminal-like labels) were located in the supra- and infragranular layers. V4 injections of CTb resulted in labeling of the thin stripes and interstripes of V2 and provided an efficient method of distinguishing the V2 modules that were related to the ventral stream from the CytOx-rich thick stripes, related to the dorsal stream. In V2, there was a significant heterogeneity in the distribution of projections: feedforward projections were located in CytOx-rich thin stripes and in the CytOx-poor interstripes, whereas the feedback projections were more abundant in the thin stripes than in the interstripes. J. Comp. Neurol. 522:3091–3105, 2014.

Do tufted capuchin monkeys play the odds? Flexible risk preferences in Sapajus spp.

As humans, several non-human animal species avoid risk, defined as "variability in rate of gain". However, non-human primate studies revealed a more complicated picture, with different species ranging from risk aversion to risk proneness. Within an ecological rationality framework, a species' feeding ecology should influence its risk preferences, as it has been shown in bonobos and chimpanzees. Although the feeding ecology hypothesis is promising, it has not been yet verified in species other than apes. Here, we aimed to assess whether this hypothesis holds true in tufted capuchin monkeys (Sapajus spp.). Ten capuchins were presented with choices between a "safe" option and a "risky" option in three conditions differing for the probability of receiving the larger reward when selecting the risky option. Similarly to chimpanzees, capuchins were risk prone. However, capuchins' behaviour was not the result of a bias towards the choice of the risky option, since-when facing options with different probabilities of obtaining the larger outcome-they were able to flexibly modify their preferences. Capuchins' decision-making under risk mirrors their risk-prone behaviour in the wild, where they often rely on unpredictable and/or hazardous food sources, thus satisfying the feeding ecology hypothesis.

Claustrum projections to prefrontal cortex in the capuchin monkey (Cebus apella).

We examined the pattern of retrograde tracer distribution in the claustrum following intracortical injections into the frontal pole (area 10), and in dorsal (area 9), and ventral lateral (area 12) regions of the rostral prefrontal cortex in the tufted capuchin monkey (Cebus apella). The resulting pattern of labeled cells was assessed in relation to the three-dimensional geometry of the claustrum, as well as recent reports of claustrum-prefrontal connections in other primates. Claustrum-prefrontal projections were extensive, and largely concentrated in the ventral half of the claustrum, especially in the rostral 2/3 of the nucleus. Our data are consistent with a topographic arrangement of claustrum-cortical connections in which prefrontal and association cortices receive connections largely from the rostral and medial claustrum. Comparative aspects of claustrum-prefrontal topography across primate species and the implications of claustrum connectivity for understanding of cortical functional networks are explored, and we hypothesize that the claustrum may play a role in controlling or switching between resting state and task-associated cortical networks.

Social status, facial structure, and assertiveness in brown capuchin monkeys

Social status, facial structure, and assertiveness in brown capuchin monkeys

Responses of Primates to Landscape Change in Amazonian Land‐bridge islands—a Multi‐scale Analysis

AbstractLarge hydroelectric dams are one of the current drivers of habitat loss across Amazonian forests. We investigated how the primate community at a hydroelectric dam in Brazilian Amazonia responded to changes in the landscape and local habitat structure of land‐bridge islands after 21 yr of post‐isolation history. The Balbina Dam, constructed in 1986, inundated 3129 km2 of primary forests and created more than 3500 variable‐sized islands. We conducted primate and habitat structure surveys on 20 islands from 5 to 1815 ha, and extracted forest patch and landscape metrics for each island. The number of primate species per island varied between 0 and 7 species. Primate composition varied substantially according to both island area and forest cover remaining within the landscape, whereas island area alone was the most significant predictor of richness. Locally, tree density and vertical stratification were the most significant explanatory variables of primate composition and richness. A model containing area effects had the most explanatory power regarding site occupancy for most species. Individually, each species responded differently, with howler and brown capuchin monkeys showing greater tolerance to cope with habitat changes. Body size was also an important predictor of primate occupancy. We recommend protecting large fragments and enhancing the suitability of surrounding habitats to ensure primate conservation in most Neotropical fragmented landscapes. Given the flat topography of hydroelectric reservoirs, which mainly favors the formation of small islands, and the escalating hydropower development plans in Amazonia, our findings provide evidence for pervasive detrimental impacts of dams on primate communities.

Does own experience affect perception of others' actions in capuchin monkeys (Cebus apella)?

Anticipating another's actions is an important ability in social animals. Recent research suggests that in human adults and infants one's own action experience facilitates understanding and anticipation of others' actions. We investigated the link between first-person experience and perception of another's action in adult tufted capuchin monkeys (Sapajus apella spp., formerly Cebus apella spp.). In Experiment 1, the monkeys observed a familiar human (actor) trying to open a container using either a familiar or an unfamiliar action. They looked for longer when the actor tried to open the container using a familiar action. In Experiment 2, the actor performed two novel actions on a new container. The monkeys looked equally at the two actions. In Experiment 3, the monkeys were trained to open the container using one of the novel actions in Experiment 2. After training, we repeated the same procedure as in Experiment 2. The monkeys looked for longer when the actor manipulated the container using the action they had practiced than when she used the unfamiliar action. These results show that knowledge derived from one's own experience impacts perception of another's action in these New World monkeys.

Competition-induced stress does not explain deceptive alarm calling in tufted capuchin monkeys

Tactical deception has long attracted interest because it is often assumed to entail complex cognitive mechanisms. However, systematic evidence of tactical deception is rare and no study has attempted to determine whether such behaviours may be underpinned by relatively simple mechanisms. This study examined whether deceptive alarm calling among wild tufted capuchin monkeys, Cebus apella nigritus, feeding on contestable food resources can be potentially explained by a physiological mechanism, namely increased activation in the adrenocortex and the resulting production of glucocorticoids (GCs; ‘stress hormones’). This was tested experimentally in Iguazu National Park, Argentina, by manipulating the potential for contest competition over food and noninvasively monitoring GC production through analysis of faecal hormone metabolites. If deceptive false alarms are indeed associated with adrenocortical activity, it was predicted that the patterns of production of these calls would match the patterns of GC output, generally being higher in callers than noncallers in cases in which food is most contestable, and specifically being higher in callers on those occasions when a deceptive false alarm was produced. This hypothesis was not supported, as (1) GC output was significantly lower in association with the experimental introduction of contestable resources than in natural contexts wherein the potential for contest is lower, (2) within experimental contexts, there was a nonsignificant tendency for noncallers to show higher GC output than callers when food was most contestable, and (3) individuals did not show higher GC levels in cases in which they produced deceptive alarms relative to cases in which they did not. A learned association between the production of alarms and increased access to food may be the most likely cognitive explanation for this case of tactical deception, although unexplored physiological mechanisms also remain possible.

Correction: Give What You Get: Capuchin Monkeys (Cebus apella) and 4-Year-Old Children Pay Forward Positive and Negative Outcomes to Conspecifics

Correction: Give What You Get: Capuchin Monkeys (Cebus apella) and 4-Year-Old Children Pay Forward Positive and Negative Outcomes to Conspecifics

Calculated reciprocity? A comparative test with six primate species.

Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject's tendency to provide food to a partner was directly affected by the partner's previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects' probability to pull was not affected by the previous number of the partner's pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.

Efferent projections of the suprachiasmatic nucleus based on the distribution of vasoactive intestinal peptide (VIP) and arginine vasopressin (AVP) immunoreactive fibers in the hypothalamus of Sapajus apella

The suprachiasmatic nucleus (SCN), which is considered to be the master circadian clock in mammals, establishes biological rhythms of approximately 24h that several organs exhibit. One aspect relevant to the study of the neurofunctional features of biological rhythmicity is the identification of communication pathways between the SCN and other brain areas. As a result, SCN efferent projections have been investigated in several species, including rodents and a few primates. The fibers originating from the two main intrinsic fiber subpopulations, one producing vasoactive intestinal peptide (VIP) and the other producing arginine vasopressin (AVP), exhibit morphological traits that distinguish them from fibers that originate from other brain areas. This distinction provides a parameter to study SCN efferent projections. In this study, we mapped VIP (VIP-ir) and AVP (AVP-ir) immunoreactive (ir) fibers and endings in the hypothalamus of the primate Sapajus apella via immunohistochemical and morphologic study. Regarding the fiber distribution pattern, AVP-ir and VIP-ir fibers were identified in regions of the tuberal hypothalamic area, retrochiasmatic area, lateral hypothalamic area, and anterior hypothalamic area. VIP-ir and AVP-ir fibers coexisted in several hypothalamic areas; however, AVP-ir fibers were predominant over VIP-ir fibers in the posterior hypothalamus and medial periventricular area. This distribution pattern and the receiving hypothalamic areas of the VIP-ir and AVP-ir fibers, which shared similar morphological features with those found in SCN, were similar to the patterns observed in diurnal and nocturnal animals. This finding supports the conservative nature of this feature among different species. Morphometric analysis of SCN intrinsic neurons indicated homogeneity in the size of VIP-ir neurons in the SCN ventral portion and heterogeneity in the size of two subpopulations of AVP-ir neurons in the SCN dorsal portion. The distribution of fibers and morphometric features of these neuronal populations are described and compared with those of other species in the present study.

Insights into Intraspecies Variation in Primate Prosocial Behavior: Capuchins (Cebus apella) Fail to Show Prosociality on a Touchscreen Task.

Over the past decade, many researchers have used food donation tasks to test whether nonhuman primates show human-like patterns of prosocial behavior in experimental settings. Although these tasks are elegant in their simplicity, performance within and across species is difficult to explain under a unified theoretical framework. Here, we attempt to better understand variation in prosociality by examining the circumstances that promote and hinder the expression of prosocial preferences. To this end, we tested whether capuchin monkeys (Cebus apella)—a species that has previously demonstrated prosocial preferences—would behave prosocially using a novel touchscreen task. In contrast to previous studies, we found that capuchins as a group did not prosocially deliver food to a partner. Importantly however, data from control conditions revealed that subjects demonstrated limited understanding of the reward contingencies of the task. We also compared individuals’ performance in the current study with their performance in a previously published prosociality study. We conclude by discussing how continuing to explore intraspecies variation in performance on prosocial tasks may help inform debates regarding the existence of other-regarding preferences in nonhuman species.

Facial width-to-height ratio relates to alpha status and assertive personality in capuchin monkeys.

Social dominance hierarchies play a pivotal role in shaping the behaviour of many species, and sex differences within these hierarchies often exist. To date, however, few physical markers of dominance have been identified. Such markers would be valuable in terms of understanding the etiology of dominant behaviour and changes in social hierarchies over time. Animals may also use such traits to evaluate the potential dominance of others relative to themselves (i.e. a physical “cue”). Facial width-to-height ratio (fWHR), for example, has been suggested as a cue to dominance in humans, with links to both dominant behaviour and the perception of dominance in other individuals. Whether this association is present in non-human animals is currently not known. Therefore, here we examine within-species links between fWHR and dominant behaviour in 64 brown capuchin monkeys (Sapajus spp.) aged between 2 and 40 years. fWHR was positively associated with alpha status and with a dimensional rating of assertive personality in both males and females. Moreover, fWHR showed significant sexual dimorphism in adults but not juveniles, suggesting a developmental change may occur during puberty. In a sub-sample, sex differences were mediated by weight, suggesting fWHR dimorphism does not exceed what would be expected by differences in body weight. This is the first report of an association between face shape and behaviour in a non-human species. Results are discussed in terms of the role that face-behaviour associations might play within capuchin societies, and the possible selective forces that might have led to the evolution of fWHR-dominance associations in humans.

Scaling the primate lateral geniculate nucleus: Niche and neurodevelopment in the regulation of magnocellular and parvocellular cell number and nucleus volume

New stereological assessments of lateral geniculate nucleus (LGN) neuron numbers and volumes in five New World primates (Cebus apella, Saguinus midas niger, Alouatta caraya, Aotus azarae, and Callicebus moloch) and compiled LGN volumes for an additional 26 mammals were analyzed for a better understanding of visual system evolution. Both the magnocellular (M)- and the parvocellular (P)-cell populations scale allometrically with brain volume in primates, P cells with a significantly higher slope such that, for every increase in M neuron number, P neuron numbers more than double (ln scale; y = 0.89x + 2.42R(2) = 0.664). In diurnal primates, the ratio of P to M cells was slightly but significantly higher than in nocturnal primates. For all mammals, including primates, LGN volume was unrelated to nocturnal or diurnal niche but showed marked differences in slope and intercept depending on taxonomic group. The allometric scaling of M and P cells can be related to the order of neurogenesis, with late-generated P cells increasing with positive allometry compared with the earlier-generated M cells. This developmental regularity links relative foveal representation to relative isocortex enlargement, which is also generated late. The small increase in the P/M cell ratio in diurnal primates may result from increased developmental neuron loss in the M-cell population as it competes for limited termination zones in primary visual cortex.