Wild capuchins (Cebus capucinus) fail to use tools in an experimental field study

From September through November 2000 we conducted an experimental field study of tool use in a group of 15 wild white-faced capuchins (Cebus capucinus) in Costa Rica. The problem presented to the capuchins involved the use of wooden dowels as probes to obtain a food reward (two bananas) located inside a clear Plexiglas box. Specifically, the task required the capuchins to manually insert a dowel into any of six holes drilled into the box in order to push the bananas off a shelf. The banana could then be retrieved through a large opening at the bottom of the box. The capuchins visited the tool-use platform 702 times over the course of 55 consecutive days and under several experimental conditions. During the first 21 days of the study, they explored the box but made no attempt to touch or pick up the dowels. Even after we placed the dowels in the holes, the capuchins only occasionally manipulated them. Overall, the results indicate that the capuchins did not use a tool to solve this novel foraging problem.     

The stone tools of capuchins (Cebus apella)

We examined the production of stone took by capuchins (Cebus apella). Eleven subjects used five reduction techniques to produce 346 stone tools (48 cores and 298 flakes). They produced a sharp edge on 83% of the cores and largest flakes. Three monkeys later used a sample of these objects as cutting tools. These results demonstrate that monkeys produce lithic tools analogous to those produced by Oldowan hominids.     

Object-use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica

Chimpanzees and capuchins demonstrate greater varieties and higher rates of tool-use when compared to other non-human primates. Although capuchins have been studied extensively in captivity, data on their tool-using behavior under free-ranging conditions are limited. This is the first long-term field research to systematically study complex object manipulation in capuchins. The aims of this research are 1) to examine the types, rates, and contexts of tool- and object-use in free-ranging capuchins and 2) to determine if free-ranging capuchins' object manipulation behavior is comparable to the behavior exhibited by captive individuals. Data on 3 troops of white-faced capuchins (Cebus capucinus) were collected from February 1995 to January 1996 at Palo Verde, Costa Rica. Data were collected using focal animal and ad libitum sampling techniques. Any observed incident of tool-use and object-use was recorded. No tool-use was observed during the 11-month study. Object-use (pound, rub, and fulcrum-use) occurred at a rate of 0.19/hr and made up less than 1% of the monkeys' time (there were no differences among the age/sex classes). The results indicate that free-ranging capuchins do not exhibit the range of tool-using behavior demonstrated by their captive counterparts. This may be the result of differential motivational responses to objects, arboreal lifestyle, absence of adequate tool material, and/or absence of food resources that require extraction involving tool-use. Am J Phys Anthropol 106:311–321, 1998. © 1998 Wiley-Liss, Inc.     

Transfer of tools and food between groups of tufted capuchins (Cebus apella)

This research examined tool and food transfer between two groups of tufted capcuhin monkeys (Cebus apella). Subjects in one group transferred stones to subjects in a second group who in turn used the stones as cutting tools and then transferred food to subjects in the first group. Aspects of the capuchins' behavior are similar to those described for food-sharing in Cebus, cooperative tool use in Papio, and tool and food exchange in Pan. We propose that tool use and food-sharing facilitate tool and food transfer between captive groups of Cebus apella. Am. J. Primatol. 43:33–41, 1997. © 1997 Wiley-Liss, Inc.     

Early behavioral development in capuchins (Cebus)

Capuchin infants (genus Cebus) are born in a behaviorally more altricial state than is known for infants of other primate taxa except apes. Development in the first 2 months after birth is characterized by the major reorganization of sleeping and waking, assumption of postural control and the appearance of prehension. Capuchins develop postural control, prehension and locomotion later than do squirrel monkeys, baboons or macaques, presenting a pattern of motor development intermediate between these relatively more precocial genera and apes. Capuchins provide a useful model primate system in which to study development and its links with behavioral variability and life history.     

Sexual behavior in brown capuchins (Cebus apella)

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Reconciliation in wild white-faced capuchins (Cebus capucinus)

The likelihood of reconciliation (defined as preferential peaceful contact among former opponents following conflicts) has been predicted to vary positively with relationship value and compatibility, and negatively with relationship security. Long-term data on wild white-faced capuchins (Cebus capucinus) indicate that dyads consisting of an adult female and an alpha male have high value and compatibility, but low security. Two studies of C. capucinus postconflict (PC) behavior were carried out at Lomas Barbudal Biological Reserve, Costa Rica. One study consisted of 30-min PC and matched control (MC) follows. The second study extracted PC and MC periods from long follows, yielding PC/MC periods averaging 105 min. In study 2, but not study 1, significantly more PC/MC pairs were attracted (former opponents affiliated with each other sooner in the PC period than in the MC period) than were dispersed (former opponents affiliated with each other sooner in the MC period than in the PC period). Reconciliation in study 2 could not be explained as a by-product of former opponents' tendency to seek affiliative contact with conspecifics generally, or of the spatial proximity of opponents following conflicts. Attempted reconciliation was less likely to be followed by renewed aggression when reconciliation attempts were delayed following conflicts. The data were insufficient for a formal test of differences in conciliatory tendency (the difference between the number of attracted and dispersed PC/MC pairs, divided by the total number of pairs) among dyad types to be conducted.     

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.     

Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

Milk composition of captive tufted capuchins (Cebus apella)

Little is known about the milk composition of nonhuman primates, and it has never been examined in capuchin monkeys (genus Cebus). This article reports on the macronutrient milk composition (fat, crude protein (CP), lactose, dry matter (DM), and total gross energy (GE)) of captive housed tufted capuchins (Cebus apella) (n=8). C. apella milk averaged 5.22% fat, 2.40% CP, 6.94% lactose, 16.48% DM, and 0.89 kcal/g. Fat was the most variable macronutrient and was significantly higher in samples collected after 2 months of lactation. To explore the adaptive significance of C. apella milk composition, results were compared with data on milk composition from a closely related cebid, Saimiri boliviensis boliviensis, and another large‐brained anthropoid, Homo sapiens. C. apella milk was only significantly different from Saimiri milk in CP and the proportion of energy from CP. Compared with human milk, C. apella milk was lower in lactose but higher in fat, CP, DM, GE, and the proportion of energy from CP. Results from this small dataset suggest that among anthropoid primates, the macronutrient composition of milk is influenced by phylogeny, may vary relative to infant growth rates, but may not be related in any direct way to relative brain size. Am. J. Primatol. 72:81–86, 2010. © 2009 Wiley‐Liss, Inc.     

Reunion displays in captive male brown capuchins (Cebus apella)

Separation and subsequent reintroduction of brown capuchins (Cebus apella) can lead to reunion displays during which individuals will embrace and emit high-pitched, loud vocalizations. These displays were investigated in three male capuchins: two adults and one juvenile. These subjects were part of a larger captive social group held at the Capuchin Laboratory, Hiram College, OH, USA. We hypothesized that males would engage in reunion displays following separation regardless of the order of reintroduction, as evidence of an affiliative bond judged by concurrent social behavior. Sixty separations were conducted as part of weekly husbandry over a period of 13 months. Occurrence of reunion displays between the males was recorded with the initiator also noted. Reunion displays among males were found to occur only between the juvenile and alpha male, and all displays were initiated by the juvenile. Displays were highly influenced by the order of reintroduction. We suggest that reunion displays operate to reaffirm social relationships, particularly during situations of social tension.     

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.     

Exposure to rabies virus in a population of free-ranging capuchin monkeys (Cebus apella nigritus) in a fragmented, environmentally protected area in southeastern Brazil

The aim of this study is to assess the frequency of rabies antibodies in free-ranging capuchin monkeys (Cebus apella nigritus) in a fragmented, environmentally protected, rural area of southeastern Brazil. Thirty-six free-ranging monkeys were tested by the rapid fluorescent focus inhibition test for detection of antibodies against rabies virus. Four individuals (11.11 %) had neutralizing antibody titers ≥ 0.25 IU/mL, demonstrating rabies virus exposure.     

Sleeping site preferences in tufted capuchin monkeys (Cebus apella nigritus)

The characteristics and availability of the sleeping sites used by a group of 27 tufted capuchin monkeys (Cebus apella nigritus) were studied during 17 months at the Iguazu National Park, Argentina. We tested different hypotheses regarding possible ultimate causes of sleeping-site selection. Most sleeping sites were located in areas of tall, mature forest. Of the 34 sleeping sites the monkeys used during 203 nights, five were more frequently used than the others (more than 20 times each, constituting 67% of the nights). Four species of tree (Peltophorum dubium, Parapiptadenia rigida, Copaifera langsdorfii and Cordia trichotoma) were the most frequently used. They constituted 82% of all the trees used, though they represent only 12% of the trees within the monkeys' home range which had a diameter at breast height (DBH) > 48.16 cm (1 SD below the mean DBH of sleeping trees). The sleeping trees share a set of characteristics not found in other trees: they are tall emergent (mean height +/- SD = 31.1+/-5.2 m) with large DBH (78.5+/-30.3 cm), they have large crown diameter (14+/-5.5 m), and they have many horizontal branches and forks. Adult females usually slept with their kin and infants, while peripheral adult males sometimes slept alone in nearby trees. We reject parasite avoidance as an adaptive explanation for the pattern of sleeping site use. Our results and those from other studies suggest that predation avoidance is a predominant factor driving sleeping site preferences. The patterns of aggregation at night and the preference for trees with low probability of shedding branches suggest that social preferences and safety from falling during windy nights may also affect sleeping tree selection. The importance of other factors, such as seeking comfort and maintaining group cohesion, was not supported by our results. Other capuchin populations show different sleeping habits which can be explained by differences in forest structure and by demographic differences.     

Reproductive Socioecology of Tufted Capuchins (Cebus apella nigritus) in Northeastern Argentina

We describe the reproductive parameters of tufted capuchins (Cebus apella nigritus) in the Iguazú National Park, NE Argentina. We obtained data on six different groups (33 individually recognized adult females) studied for periods of 2–9 years. Estimated birthrate is 0.59 infants per female per year in unprovisioned groups. A group that was provisioned for 6 years during the winter period of low fruit availability (May–August), showed a similar birth rate of 0.61, but a lower infant mortality rate than unprovisioned groups. The birthrate estimated for this population is higher than the one reported for white-faced and wedge-capped capuchins. The mean interbirth interval is 19.35 months, but a female can have infants in successive years, even when her previous infant has survived. The modal age at first delivery is 7 years, which is similar to the one observed in wedge-capped capuchins. When young adult females come into estrous they avoid copulating with the alpha male that sired them, thus providing evidence for a behavioral mechanism of inbreeding avoidance. Births are very seasonal at Iguazú, occurring during the spring and summer months (October–February) when food availability is at its peak. Tufted capuchins at Iguazú are more seasonal breeders than other capuchin populations, probably as a result of their more seasonal environment. The secondary sex ratio does not deviate significantly from 1:1, despite the known ability of capuchins to adjust secondary sex ratio to local conditions.     

Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus)

Researchers have identified a variety of cross-site differences in the foraging behavior of free-ranging great apes, most notably among chimpanzees (Pan troglodytes) and more recently orangutans (Pongo pygmaeus), that are not due to obvious genetic or ecological differences. These differences are often referred to as "traditions." What is not known is whether this high level of interpopulation variation in behavior is limited to hominoids. In this study, we use long-term data from three Costa Rican field sites that are geographically close and similar ecologically to identify potential foraging traditions in white-faced capuchins (Cebus capucinus). Foraging traditions are predicted in Cebus because of many behavioral and morphological convergences between this genus and the great apes. The processing techniques used for the same food species were compared across sites, and all differences found were classified as present, habitual, or customary. Proximity data were also analyzed to determine if social learning mechanisms could explain variation in foraging behavior. Of the 61 foods compared, we found that 20 of them are processed differently by capuchins across sites. The differences involve pound, rub, tap, "fulcrum," "leaf-wrap," and "army ant following." For most of the differences with enough data to analyze, the average proximity score of the "matched" dyads (two individuals within a group who shared a "different" processing technique) was statistically higher than the average proximity score of the remaining "unmatched" dyads.     

Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus)

In many primate species, conspicuous behavioral and/or morphological changes are indicators of the fertile phase of the female cycle. However, several primate species, such as the white-faced capuchin, lack these cues. This is referred to as "concealed ovulation," and is argued to be a reproductive strategy that confuses paternity and lowers the risk of infanticide. We studied 10 adult female white-faced capuchins in Santa Rosa National Park, Costa Rica, from January to June 2002. We determined their ovarian cycling patterns by analyzing fecal ovarian hormones, and compared simultaneously collected behavioral data to determine which, if any, cues females use to signal their fertile phases. We found that four females cycled during the study period but ceased to cycle without becoming pregnant. We considered several explanations for the lack of conception during our study, including reproductive seasonality. We found that female C. capucinus showed only small increases in rates of affiliative/proceptive behaviors directed toward adult males during their periovulatory phases. The best indicator of cycle phase was a significant increase in male affiliative behaviors (e.g., following and grooming bouts) and sexual behaviors (e.g., copulations and courtship displays) directed toward females during the periovulatory phase compared to the nonovulatory phase. Our finding that females exhibit little proceptive behavior, but that copulations and male courtship are nonetheless concentrated in periovulatory phases suggests that even though females do not provide behavioral and morphological cues to ovulation, males are still able to detect it. Infanticide occurs with some frequency in these monkeys, and there is evidence for postconceptive mating as a female strategy to lower risk of infanticide via paternity confusion. However, despite this occurrence of nonconceptive mating and the absence of female cues to ovulation, truly concealed ovulation does not appear to be characteristic of this study population of white-faced capuchins.