Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.     

Aggression and Reconciliation in Cebus capucinus

Most data relating to aggressive and conciliatory behaviors are from Old World primates. We recorded agonistic interactions and post-conflict behaviors in a group of 12 white-faced capuchins (Cebus capucinus). After a conflict, we followed the aggressee as the focal individual during a 10-min postconflict period. We also conducted matched-control observations on the same individual. Conflicts involving physical contact were significantly bidirectional, and conflicts without physical contact were preferably unidirectional. Reconciliation was not be demonstrated at the group level. However, reconciliation occurred in kin and non-kin male/female dyads: their conciliatory tendencies were 48.1% and 21.2%, respectively. White-faced capuchins reconciled mainly during the first minutes after the end of the conflict. In kin and non-kin male/female dyads, selective attraction occurred, and aggressors were more likely to initiate affiliative contacts than aggressees. Hold-bottom and mount while emitting loud vocalizations were the most characteristic behaviors of reconciliation. Possible links may exist between aggressive and conciliatory patterns and other social variables.     

Hyperprogesteronemia in response to Vitex fischeri consumption in wild chimpanzees (Pan troglodytes schweinfurthii)

Chimpanzees in Gombe National Park consume fruits of Vitex fischeri during a short annual fruiting season. This fruit species is a member of a genus widely studied for phytoestrogen composition and varied physiological effects. One particularly well-studied species, V. agnus-castus, is noted for its documented effects on female reproductive function, evidenced in increased progesterone levels and consequent regulation of luteal function. We examined reproductive hormone levels in both male and female chimpanzees during a 6-week period of intense V. fischeri consumption. V. fischeri consumption was associated with an abrupt and dramatic increase in urinary progesterone levels of female chimpanzees to levels far exceeding the normal range of variation. Female estrogen levels were not significantly impacted, nor were male testosterone levels. These are some of the first data indicating that phytochemicals in the natural diet of a primate can have significant impacts on the endocrine system, though the fluctuating nature of chimpanzee diet and reproductive function does not allow us to determine whether the effects observed during this short period had a broader positive or negative impact on female fertility. Given the widespread use of various Vitex species by African primates and the as-yet-undescribed phytochemical properties of these species, we predict that our observations may be indicative of a broader phenomenon.     

Response Toward Novel Foods and Novel Objects in Wild Cebus apella

Animals respond to novel stimuli via explorative or neophobic behavior or both. The coexistence of these responses toward novel foods may be a successful adaptive strategy for a generalist species such as Cebus apella, because it allows the gradual introduction of new foods into the diet and reduces the risk of poisoning by ingestion of large amounts of toxic compounds (Glander, 1982; Milton, 1993; Visalberghi, 1994). Neophobia has been studied mostly in captivity. We investigated responsiveness to novelty in a group of 25–30 wild tufted capuchins (Cebus apella) in Iguazü National Park (Argentina). They had been habituated to visiting sites where bananas were provided on three elevated platforms. We presented novel stimuli on an adjacent platform. There were 4 experimental conditions with 10 sessions each: the Novel Food condition, the Novel Object condition, the Control condition, in which the platform was empty, and the Banana condition. In the Novel Food and Novel Object conditions, a new stimulus—food or object—was on the platform during each session. The Banana condition provided information on capuchin response to a familiar preferred food. Overall, capuchins were less responsive toward novel objects than toward novel foods; however, although cautious, they ate small amounts of the novel foods. Age affected individual responsiveness toward novel foods, whereas sex affected responsiveness toward novel objects. Capuchins ignored the empty platform. Our findings are in agreement with the idea that tufted capuchins can adapt to new habitats by gradually exploiting new food sources.     

Hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella)

The purpose of this study was to examine the hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella). Two experiments were conducted. In Experiment 1 capuchins were presented with an apparatus designed to accommodate the use of probing tools. In Experiment 2 the same capuchins were presented with sets of nesting containers. Five of the ten subjects used probing tools and seven subjects placed objects in the containers. The capuchins' behavior reflected three hierarchically organized combinatorial patterns displayed by chimpanzees and human infants. Although the capuchins sometimes displayed the two more complex patterns (“pot” and “subassembly”), their combinatorial behavior was dominated by the simplest pattern (“pairing”). In this regard capuchins may not attain the same grammar of manipulative action that has been reported for chimpanzees and young human children. © 1994 Wiley-Liss, Inc.     

The relationship between locomotor behavior and limb morphology in brown (Cebus apella) and weeper (Cebus olivaceus) capuchins

This study is a comparison of locomotor behavior and postcranial form in two species of capuchin monkey, the brown capuchin (Cebus apella), and the weeper capuchin (Cebus olivaceus). Behavioral data from groups of wild C. apella and C. olivaceus in Guyana were collected during the period of December 1999 through November 2000. Postcranial variables including 40 measurements and three indices were taken from 43 adult and subadult specimens of C. apella and 14 adult and subadult specimens of C. olivaceus housed in American museums, as well as two wild-caught adult specimens of C. olivaceus from the Georgetown Zoo in Guyana. The results of this study indicate that these two capuchins exhibit similar patterns of locomotor behavior, but that there are important differences in how they move through their homerange, particularly with respect to quadrupedalism. These differences in behavior are reflected in their postcranial morphology and can be related to differences in foraging strategies. This study provides an example of the importance of using more exclusive categories of quadrupedal behaviors when comparing closely related arboreal quadrupeds, as well as an alternative explanation for some of the postcranial features of C. apella that may relate to foraging postures and foraging strategy rather than traditionally categorized patterns of locomotor behavior.     

Vertebrate Predation and Food-Sharing in Cebus and Pan

Capuchins and chimpanzees are the only nonhuman primates apart from baboons known to prey systematically upon relatively large vertebrates. Vertebrate predation is common and well documented in Pan troglodytes, rare in Pan paniscus, and commonly reported but infrequently studied in Cebus. Food-sharing is common in both Pan species but rarely reported for wild capuchins. I present data on vertebrate predation and food-sharing by white-faced capuchins (Cebus capucinus) from ongoing field studies at Santa Rosa National Park, Costa Rica. We have observed 106 successful predation events resulting in the capture of 156 prey items during 2929 observation hr (5.35 prey per 100 hr). Squirrels and nestling coatis comprised half of the prey taken; the remainder were mainly nestling birds and eggs. Adult males took 52% of all prey and 67% of squirrels. Squirrels are actively hunted and about 65% of them are adults. I estimated that the average capuchin group kills 43–50 squirrels annually, mostly during the dry season. Capuchins hunt squirrels in groups 81% of the time, and 17% of hunts are successful. There is no evidence for cooperative hunting, but occasional collaboration is suggested. Rates of food-sharing were low (1.7 per 100 hr), and meat was the only food shared between adults. I compare predation and food-sharing in C. capucinus with published data for Pan troglodytes, primarily in Gombe and Taï National Parks. I discuss sex differences, hunting strategies, the relationship between hunting and food-sharing, and various ecological and social factors that may promote vertebrate predation in Pan and Cebus.     

Life History Variation in Female Gambusia hubbsi

Gambusia hubbsi populations occur in a variety of fresh and brackish-water habitats on Andros, Bahamas. These include shallow water sites (tidal creeks, lakes, roadside ditches), and blueholes (vertical solution caves). In some blueholes G. hubbsi is the only species present, in others it co-occurs with other species, principal among these is a predator, Eleotris pisonis. By contrast to blueholes, shallow water sites have highly variable temperature and depth. In addition, they are frequented by avian piscivores and may be occasionally occupied by piscivores such as Eleotris. We sampled 10 shallow water sites, 14 blueholes where Eleotris is absent and 12 blueholes where Eleotris co-occurs with G. hubbsi. We measured and compared variation in female body size, fecundity, and reproductive investment among these three habitats. The observed patterns of life history variation are only partially in accord with expectations from theory regarding the effects of predation and seasonality on life history variation. Samples from populations that colonized a series of man-made trenches (Well Fields), a set of introductions into that habitat, and changes in life history traits of lab-raised females from three blueholes, suggest that the observed pattern of life history variation in other habitats also reflects differences in food availability among habitats, and imperfectly reflects the potential phenotypic variability of this species.     

Growth and reproduction in captive tufted capuchins (Cebus apella)

We present data on weight and reproduction from a colony of tufted capuchins monkeys (Cebus apella) over a 12 year period. The data constitute a normative record for this species. Weight at birth averages 210 g, and infants gain weight rapidly. Females typically first conceived just after their fifth birthday, and males were fertile by 4 years, 5 months. Interbirth intervals average 576 days. Eighty-seven percent of live-born infants survived past 6 months. Three of eight live-born infants that died prior to 6 months succumbed from trauma inflicted by cage mates. Am. J. Primatol. 44:197–203, 1998. © 1998 Wiley-Liss, Inc.     

Capuchin (Cebus apella) Tool Use in a Captive Naturalistic Environment

Captive tufted capuchins are proficient at both tool use and manufacture. However, their capacity to comprehend cause-effect relationships as they relate to tool use is a subject of debate. An ability to conceptualize task requirements in assessing the appropriateness of potential tools would be essential to efficient tool use in the wild. Observations of tool use among free-ranging populations of Cebus are extremely limited, and the importance of this behavior to capuchin feeding ecology is unclear. I tested tufted capuchins' ability to conceive solutions to a probing task in a naturalistic captive setting. Three out of 5 participants demonstrated an ability to consistently make and use tools selected from a wide variety of natural materials within a forest exhibit. Over 98% (N = 140) of the tools that they modified enabled them to successfully acquire food rewards. It is likely that wild Cebus apella shares this ability, and that tool use occurs under a highly specific set of natural conditions.     

A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest,Zaire, and Pan troglodytes in the Kibale Forest,Uganda

Differences in the social organization and dental morphology of Pan paniscus (bonobos) and Pan troglodytes (chimpanzees) have been related to differences in the spatiotemporal availability of food and its exploitation. The presence of abundant terrestrial herbaceous vegetation (THV) in the bonobo's habitat and the apparent greater reliance on herbs for food has been used to explain differences in party size and, by extension, social organization. Using fecal analysis, we assess quantitatively the amount of herbaceous foods consumed by Pan paniscus in the Lomako Forest, Zaire, compared to similar data for Pan troglodytes in the Kibale Forest, Uganda. We examine this data in the context of spatiotemporal patterns of availability of herbaceous foods and fruit, as well as their nutritional content. The results support the suggestion that bonobos consume more herbaceous food than do the Kibale chimpanzees and that these foods are more prevalent in the bonobo's habitat than in the Kibale Forest. However, temporal changes in fruit availability and herb consumption, along with nutritional analyses, suggest that chimpanzees consume herbs as a fallback source of carbohydrates, whereas bonobos consume herbs as a source of protein regardless of season or fruit abundance. Available data suggest that party size while feeding on terrestrial herbs is restricted at both sites, but a determination of the relative strength of this constraint is not possible at this time. Difficulties in methods used for data collection are discussed and areas where more information is needed are highlighted. © 1994 Wiley-Liss, Inc.     

Volumetric and lateralized differences in selected brain regions of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus)

The two species of Pan, bonobos and common chimpanzees, have been reported to have different social organization, cognitive and linguistic abilities and motor skill, despite their close biological relationship. Here, we examined whether bonobos and chimpanzee differ in selected brain regions that may map to these different social and cognitive abilities. Eight chimpanzees and eight bonobos matched on age, sex and rearing experiences were magnetic resonance images scanned and volumetric measures were obtained for the whole brain, cerebellum, striatum, motor‐hand area, hippocampus, inferior frontal gyrus and planum temporale. Chimpanzees had significantly larger cerebellum and borderline significantly larger hippocampus and putamen, after adjusting for brain size, compared with bonobos. Bonobos showed greater leftward asymmetries in the striatum and motor‐hand area compared with chimpanzees. No significant differences in either the volume or lateralization for the so‐called language homologs were found between species. The results suggest that the two species of Pan are quite similar neurologically, though some volumetric and lateralized differences may reflect inherent differences in social organization, cognition and motor skills. Am. J. Primatol. 71:988–997, 2009. © 2009 Wiley‐Liss, Inc.     

Success and Understanding in Cognitive Tasks: A Comparison Between Cebus apella and Pan troglodytes

The recent boom in cognitive studies on chimpanzees and capuchins allows an analysis of the cognitive processes and behavioral tendencies underlying their performances when faced with a variety of problems. In the laboratory, but less so in nature, Cebus and Pan show remarkable convergence in their overall success in solving problems involving the use of tools and cooperation. Behavioral ingredients such as explorative tendencies, manipulative skills, social tolerance, and cognitive capacities contribute to their success. However, in experiments in which carefully controlled conditions were implemented, e.g., cooperation and tool-using tasks, differences between the two taxa emerged in the role played by such ingredients in fostering success. Although it is difficult to establish the nature of these differences, a profitable way to look at them is from outside: from the point of view of what children do when tested in similar tasks. If we consider the ways in which children experience or achieve initial success and then become fully proficient in solving similar tasks, we can appreciate the different recipes for success that Pan and Cebus present.     

Summation and quantity judgments of sequentially presented sets by capuchin monkeys (Cebus apella)

Capuchin monkeys (Cebus apella) were presented with two sets of food items, identical in food type but differing in number. Animals selected one set and were permitted to consume their choice. Set sizes ranged from 1 to 6 items. In experiment 1, each set was uncovered and recovered before a response was made, and the monkeys selected the larger set at high levels. Experiment 2 presented sets that had both visible and nonvisible food items in them at the time of the response, thus requiring the monkeys to sum the total amount of food that was available. The monkeys again selected the larger set with no decrement in performance. Overall, the data indicate that capuchins, like other more extensively studied primate species in this area of research, are responsive to quantitative differences between sets. Capuchins succeed in making these quantity judgments when sets are nonvisible at choice time and when summation of items must be performed, thus demonstrating coordination of quantification skills and memory. Capuchins also inhibit responses to visible food items when those items are only part of an overall smaller quantity of food compared with a completely nonvisible set.     

The effect of peer separation in young chimpanzees (Pan troglodytes)

Ten chimpanzees (Pan troglogytes), aged 18–24 months, housed without mothers as two dyads and two triads, were subjected to social separation. Two issues were addressed: the effects of peer separation in chimpanzees; and differential responses by subjects living in dyads compared with those living in triads. Chimpanzees that were alone during separation reacted with high levels of “protest” alternating with “despair” throughout the separation period. The continued presence of one cagemate, during separation from a third, was a strong mitigating factor. Even when the primary attachment was formed with the absent cagemate, the remaining chimpanzees clung to each other and the levels of protest and despair, when present, were low. Upon reunion, neither “detachment” nor heightened levels of clinging were conspicuous, but there was increased social interaction. The data on separation of chimpanzees are intermediate between those of humans and monkeys separated from mothers or peers. The increased social interactions during reunion, including looking, are comparable to the visual vigilance reported for humans.     

Social traditions and social learning in capuchin monkeys (Cebus)

Capuchin monkeys (genus Cebus) have evolutionarily converged with humans and chimpanzees in a number of ways, including large brain size, omnivory and extractive foraging, extensive cooperation and coalitionary behaviour and a reliance on social learning. Recent research has documented a richer repertoire of group-specific social conventions in the coalition-prone Cebus capucinus than in any other non-human primate species; these social rituals appear designed to test the strength of social bonds. Such diverse social conventions have not yet been noted in Cebus apella, despite extensive observation at multiple sites. The more robust and widely distributed C. apella is notable for the diversity of its tool-use repertoire, particularly in marginal habitats. Although C. capucinus does not often use tools, white-faced capuchins do specialize in foods requiring multi-step processing, and there are often multiple techniques used by different individuals within the same social group. Immatures preferentially observe foragers who are eating rare foods and hard-to-process foods. Young foragers, especially females, tend to adopt the same foraging techniques as their close associates.