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Effects of upright posture on hand preference for reaching vs. the use of probing tools by tufted capuchins (Cebus apella).

This research examined the effects of task (reaching vs. tool use) and posture (quadrupedal vs. bipedal) on hand preference in tufted capuchins (Cebus apella). Regarding direction of hand preference, we found a significant main effect of posture, as the bipedal stance elicited greater use of the right hand than did the quadrupedal stance, and a significant posture x task interaction, as bipedal reaching elicited greater use of the right hand than did other postural and task conditions. Further, we found a significant main effect of task on strength of hand preference, as tool use elicited more consistent use of one hand over the other than did reaching. Our findings indicate that bipedal reaching facilitates a mild right-hand bias in intensely manipulative primates. We speculate that this moderate bias may have been pushed in the direction of nearly exclusive right-hand preference in most humans with the development of complex tool use.

Animals↗

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.

Abortion, Veterinary↗

Environmental enrichment of brown capuchins (Cebus apella): behavioral and plasma and fecal cortisol measures of effectiveness.

No consensus exists about the quantity and variety of environmental enrichment needed to achieve an acceptable level of psychological well-being among singly housed primates. Behavioral and plasma and fecal cortisol measures were used to evaluate the effectiveness of four levels of toy and foraging enrichment provided to eight wild-caught, singly housed adult male brown capuchins (Cebus apella). The 16-week-long study comprised six conditions and began with a 4-week-long preexperimental and ended with a 4-week-long postexperimental period during which the subjects were maintained at baseline enrichment levels. During the intervening 8 weeks, the subjects were randomly assigned to a sequence of four 2-week-long experimental conditions: control (baseline conditions), toy (the addition of two plastic toys to each cage), box (access to a foraging box with food treats hidden within crushed alfalfa), and box & toy (the addition of two plastic toys and access to a foraging box). Behavioral responses to changes in enrichment were rapid and extensive. Within-subject repeated-measure ANOVAs with planned post hoc contrasts identified highly significant reductions in abnormal and undesirable behaviors (and increases in normal behaviors) as the level of enrichment increased from control to toy to box to box & toy. No significant behavioral differences were found between the control and pre- and postexperimental conditions. Plasma and fecal cortisol measures revealed a different response to changing enrichment levels. Repeated-measure ANOVA models found significant changes in both these measures across the six conditions. The planned post hoc analyses, however, while finding dramatic increases in cortisol titers in both the pre- and postexperimental conditions relative to the control condition, did not distinguish cortisol responses among the four enrichment levels. Linear regressions among weekly group means in behavioral and cortisol measures (n=16) found that plasma cortisol was significantly predicted by the proportions of both normal and abnormal behaviors; as the proportion of normal behaviors increased, the plasma cortisol measures decreased. Plasma cortisol weekly group means were also significantly and positively predicted by fecal cortisol weekly group means, but no behavioral measure significantly predicted fecal cortisol weekly group means. In sum, these findings argue strongly that access to a variety of toy and foraging enrichment positively affects behavioral and physiological responses to stress and enhances psychological well-being in singly housed brown capuchins.

Animal Welfare↗

Characterization of constitutive heterochromatin in Cebus apella (Cebidae, Primates) and Pan troglodytes (Hominidae, Primates): comparison to human chromosomes.

Using G bands, some homologies between the chromosomes of Cebus apella (CAP) and human chromosomes are difficult to establish. To solve this problem, we analyzed these homologies by fluorescence in situ hybridization using human whole chromosome probes (ZOO-FISH). The results indicated that 1) the human probe for chromosome 2 partially hybridizes with CAP chromosomes 13 and 5, 2) the human probe for chromosome 3 partially hybridizes with CAP chromosomes 18 and 20, 3) the human probe for chromosome 9 partially hybridizes with CAP chromosome 19, and 4) the human probe for chromosome 14 hybridizes with the p-terminal and q-terminal regions of CAP chromosome 6. However, none of the human probes employed hybridized with the heterochromatic regions of CAP chromosomes. For this reason, we characterized the heterochromatic regions of CAP chromosomes and of the chromosomes of Pan troglodytes (PTR), to allow comparison between CAP, PTR, and human chromosomes using in situ digestion of fixed chromosomes with the restriction enzymes AluI, HaeIII, and RsaI and by fluorescent staining with DA/DAPI. The results show that 1) centromeric heterochromatin is heterogeneous in the three species studied and 2) noncentromeric heterochromatin is homogeneous within each of the three species, but is different for each species. Thus, centromeric heterochromatin undergoes a higher degree of variability than noncentromeric heterochromatin.

Animals↗

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.

Animals↗

Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus).

Primate vocalizations that appear to occur independently of specific contexts typically are considered to be contact calls. However, results from several recent studies indicate that these calls function to facilitate social interactions. White-faced capuchin monkeys (Cebus capucinus) emit a high-frequency vocalization, termed a "trill," in social interactions and during travel. In this study, immatures emitted most trills, but adult females also trilled; by contrast, adult males rarely trilled. Infants emitted the majority of trills, and they trilled at significantly higher rates than adult females. Infants trilled most when approaching other individuals. Furthermore, infants emitted proportionately more trills than other age classes when approaching other individuals. I therefore focused on the detailed context and immediate behavioral correlates of trilling by infants. Infants that trilled when approaching others tended to interact affiliatively with them subsequently (i.e., climbing on, touching, receiving grooming, and performing food inspection) more than infants that did not trill when approaching. Therefore, infant trilling may have had an immediate effect on the recipient's behavior.

Age Factors↗

Throwing behavior and mass distribution of stone selection in tufted capuchin monkeys (Cebus apella).

Cannell [Journal of Archaeological Science 29:335-339, 2002] argued that sex-based differences among humans in terms of the mass of chosen throwing stones could be used to infer body mass and patterns of sexual dimorphism in early hominids from Olduvai and Koobi Fora by examining the mass distributions of unaltered stone tools at those sites. We examined this hypothesis in tufted capuchin monkeys using a comparative approach, by investigating the relationships among body mass, sex, stone weight preference, and accuracy in a throwing task. The subject sample consisted of nine monkeys trained to perform an aimed-throwing task in which a food reward could be obtained by throwing a stone into a bucket. We found that 1) the subjects showed a strong mean stone mass preference; 2) the females chose heavier stones than the males, in terms of absolute mean selected stone mass and selected stone mass relative to body mass; 3) subjects threw more accurately when they used stones of preferred mass vs. stones of nonpreferred mass; and 4) overall, the males were more accurate in the throwing task than the females. We conclude that capuchins are highly selective when choosing throwing stones, and that this confers an advantage for throwing accuracy. Our results indicate that the sexually dimorphic pattern in stone mass preference observed among humans does not generalize to Cebus apella. We suggest that researchers examining this pattern in humans in an attempt to explain early hominid patterns of dimorphism and behavior should take into account not only stone weight preference, but also its adaptive advantage.

Animals↗

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.

Animals↗

Birth seasonality of Cebus apella (Platyrrhini, Cebidae) in Brazilian zoos along a latitudinal gradient.

Birth seasonality in wild neotropical primates has been suggested to increase with latitude as a response to a stronger divergence in high-quality food availability across the year, and a higher between-year predictability at higher latitudes related to temporal differences in photoperiod. In captivity, however, monkeys are fed foods of similar quality throughout the year, and this consistency of diet should have a releasing effect on the need for birth seasonality. In this paper, we test whether 1) brown capuchin monkeys (Cebus apella) breed seasonally in captivity, and 2) given the consistency of diet in this setting, differences in latitude are reflected in the temporal pattern of birth distribution across the year. Data on the distribution of birth records of C. apella at Brazilian zoos located within three latitudinal zones (Equator perpendicular 8 degrees S, 16 degrees perpendicular 24 degrees S, and 24 degrees perpendicular 32 degrees S) are compared. Captive C. apella showed a birth peak from October to February, despite the consistent provision of food in this setting. In addition, there were no differences in the pattern of birth distribution among the latitudinal zones, which lends no support to the prediction that captive C. apella birth seasonality would increase with latitude. We suggest that if this species is not sensitive to subtle differences in photoperiod, other environmental cues may trigger the onset of reproduction at lower latitudes.

Animals↗

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.

Aggression↗

Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus).

Tufted capuchin monkeys (Cebus apella) provide an extreme example of active female sexual solicitation of males. In spite of being targeted by females for sex, males may delay copulation for hours or days. Data were collected on the sexual interactions in one wild capuchin group at the Estação Biológica de Caratinga in Brazil from September 1996 to August 1997. All successful conceptions during this year occurred in the dry season, yet sexual behavior was observed during 9 months of the year. This study tested whether male sexual response to female proceptivity was seasonally-mediated. Male consortship participation, solicitation of females, latency to copulation, and copulation frequency were compared between fertile and nonconceptive females. Seasonal patterns in copulation interference, mating style, and alternative mating strategies were also examined. Thirty-two copulations were observed. The alpha male was solicited for significantly more consortship days per female, but his mating success, in terms of copulation frequency, did not differ from that of two other adult males in the group. In the dry season, when the females were fertile, the males showed increased contest competition for mates, a higher frequency of alternative mating strategies against copulation interference, and increased monitoring of the females' condition. However, contrary to expectations, the alpha male's latency to copulation was significantly longer in the fertile season than in the nonconceptive months, and no males were observed to mate more than one time per day, even at the conceptive peak. Male mating strategies were affected by both season and rank, and there was evidence for reproductive constraints on males throughout the year. Limited male ejaculatory capacity and male choice in the timing of copulations within female proceptive phases may both be important factors in driving the sexual dynamics of this species.

Animals↗

Demonstration of a genotype-phenotype correlation in the polymorphic color vision of a non-callitrichine New World monkey, capuchin (Cebus apella).

Color-vision polymorphism in New World monkeys occurs because of an allelic polymorphism of the single-copy red-green middle-to-long-wavelength-sensitive (M/LWS) opsin gene on the X chromosome. Because color-vision types can readily be estimated from allelic types of the M/LWS opsin gene, this polymorphic system offers researchers an excellent opportunity to study the association between vision and behavior. As a prerequisite for such studies, genetically determined color-vision types must be concordant with phenotypes determined directly by behavioral criteria (e.g., by a color discrimination test). However, such correlations between genotypes and phenotypes have been studied only for callitrichine species. Using genetic, electrophysiological, and behavioral approaches, we evaluated the color vision of brown capuchin monkeys (Cebus apella), a representative non-callitrichine model animal for physiology and behavior. Two allelic M/LWS opsins-P545 and P530-were identified in the studied captive population. Females had one or both of the alleles, and males had either one. The retinal sensitivity in P530 dichromats was short-wave shifted relative to that in P545 dichromats, whereas that in P530/P545 trichromats was between the two groups. In a discrimination task using Ishihara pseudo-isochromatic plates, P530/P545 trichromats were successful in discriminating stimuli that P530 and P545 dichromats were unable to discriminate. In a food-search task, P530/P545 trichromats were able to locate red targets among green distracters as quickly as among white distracters, whereas both types of dichromats took longer. These results demonstrate the mutual consistency between genotypes and phenotypes of color vision, and provide a solid genetic basis on which the ecology and evolution of color vision can be investigated.

Animals↗

Exchange, affiliation, and protective interventions in semifree-ranging brown capuchin monkeys (Cebus apella).

The "social intelligence" hypothesis proposes that intelligence evolved as a consequence of the need for behavioral maneuvering to deal with the complexities of social life. As a result, coalitions have received considerable attention. Here we present the patterns of coalitionary behavior observed in a semifree-ranging group of Cebus apella and explore the effects of kinship, spatial proximity, and rank. In contrast to descriptions of Old World monkeys and to some descriptions of capuchins, kinship did not influence the pattern of coalitionary behavior, although individuals tended to help those that remained in close proximity. Rank had the greatest influence on coalitions: those that interfered in conflicts (often the alpha) were higher ranking than both contestants and supported the most subordinate (younger) interactant. However, rank did not influence the coalitionary support when conflicts involved only adults. We found no evidence that individuals were making use of triadic knowledge, and most of the coalitions can best be described as protective interventions involving immatures. The overall low rate of coalitions may be due to a period of social stability.

Age Factors↗

Hand use by tufted capuchins (Cebus apella) to extract a small food item from a tube: digit movements, hand preference, and performance.

The aim of this study was to analyze the manual patterns used by tufted capuchin monkeys (Cebus apella) to retrieve a small food item from a narrow tube, with special attention focused on the independent use of single fingers, fine digit movements, hand preference, and intermanual differences in the time it took the monkeys to obtain the food. The capuchins (n = 20) mainly used their forefinger to extract the food from the tube. The simultaneous use of the index and middle fingers occurred less frequently, and the use of the forefinger in combination with other digits occurred rarely. The capuchins demonstrated a capacity to move single digits independently when the fingers were locating the food inside the tube, and displayed a high mobility of the distal phalanx joints. However, they possessed only a limited capacity to coordinate single fingers in space, and displayed only a slight degree of manual preshaping when they approached the tube. A hand-preference analysis failed to reveal any significant lateral bias for the group, since both adults (> or = 5 years) and immature individuals (<5 years) of both sexes used either hand with the same frequency. Conversely, a latency analysis showed a significant interaction between the subject's age and performance difference between hands: in adults, but not in immature individuals, the left hand was faster than the right hand in retrieving food.

Animals↗

Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method.

Food abundance and distribution have played a central role in the conceptual theory of primate socioecology [Janson, Behaviour 105:53-76, 1988; Isbell, Behavioral Ecology 2:143-155, 1991; Sterck et al., Behavioral Ecology and Sociobiology 41:291-309, 1997; van Schaik, In: Standen V, Foley RA, editors, Comparative Socioecology. Oxford: Blackwell. p 195-218, 1989]. This theory predicts that agonistic ("contest") competition should occur when food is distributed in discrete, defensible patches; in contrast, when food sources are distributed uniformly or randomly, non-agonistic ("scramble") competition is expected. Primatologists usually measure resource density and patchiness from a botanical perspective, ignoring the biology of the animal being studied. Such an approach may be irrelevant in terms of how animals view the dispersion of resources. Using a novel focal-tree method that measures resource availability on a scale that is both spatially and temporally relevant to the animal under investigation, we take a cost-benefit approach to predict the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus) from 11 ecological and social variables. We retained four variables in the regression model: two representing the opportunity for aggression (i.e., feeding bout length and the number of feeding adult females), and two representing opportunity costs (i.e., fruit abundance and the number of potential feeding sites in the focal tree). The results of this study indicate that the amount of food-related aggression in white-faced capuchins can be predicted by variables representing the costs and benefits of contesting a food resource.

Agonistic Behavior↗

Analysis of tufted capuchin (Cebus apella) courtship and sexual behavior repertoire: changes throughout the female cycle and female interindividual differences.

Sexual solicitations and initiative (proceptivity, sensu Beach [1976] Horm Behav 7:105-138) are important components of the sexuality of females of many primate species. In the tufted capuchin (Cebus apella), female proceptivity characterizes the species' mating system. In study 1, we defined and discussed 20 behavioral patterns based on the observation of 6 females and 5 males living in two social groups. In study 2, each behavior, including mounting activity, was quantitatively assessed during the periovulatory and nonperiovulatory cycle phases of 4 females, detected on the basis of urinary progestin levels (N = 20 ovulatory cycles, 5 for each female); moreover, we monitored changes in females' social interactions (agonism, grooming activity, and play). Nine of the behaviors typically used by the female during courtship and in sexual interactions showed a dramatic increase during the periovulatory phase. Though males mounted females at an apparently higher rate during the periovulatory than the nonperiovulatory phase, the difference was not significant. However, when adult male mounting is separated into those which occur within play and nonplay contexts, there is a significant periovulatory phase effect for mounts not associated with play. Females groomed adult males at the same rate throughout the cycle. Agonism and play did not show any phase effect; however, females' avoidance of adult males significantly increased during the periovulatory phase. Finally, each female made a statistically different use of the behavioral repertoire by performing some behaviors more than others. This variability among females during courtship calls for further research into whether it affects mating success.

Aggression↗

Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item.

This study investigates prehension in 20 tufted capuchins (Cebus apella) in a reaching task requiring individuals to grasp a small food item fixed to a tray. The aim was twofold: 1) to describe capuchins' grasping techniques in detail, focusing on digit movements and on different areas of contact between the grasping fingers; and 2) to assess the relationship between grip types and manual laterality in this species. Capuchins picked up small food items using a wide variety of grips. In particular, 16 precision grip variants and 4 power grip variants were identified. The most frequently used precision grip involved the distal lateral areas of the thumb and the index finger, while the most preferred kind of power grip involved the thumb and the palm, with the thumb being enclosed by the other fingers. Immature capuchins picked up small food items using power grips more often than precision grips, while adult individuals exhibited no significant preference for either grip type. The analysis performed on the time capuchins took to grasp the food and withdraw it from the tray hole revealed that 1) precision grips were as efficient as power grips; 2) for precision grips, the left hand was faster than the right hand; and 3) for power grips, both hands were equally quick. Hand preference analysis, based on the frequency for the use of either hand for grasping actions, revealed no significant hand bias at group level. Likewise, there was no significant relationship between grip type and hand preference.

Animals↗

Cerebral venous hemodynamics and the basicranium of Cebus.

The study of basicranial foramina has played an important role in primatological investigations. They are often the only clues for deciphering cerebral vascular evolution in fossil forms. This study illustrates the significance of considering foraminal shape when analyzing or describing basicranial anatomy in living and fossil primates. It is suggested that certain hemodynamic properties of cerebral venous drainage in Cebus represent patterns that were most likely present in ancestral catarrhines.

Animals↗