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.     

Introduction and integration of strangers into captive groups of tufted capuchins (Cebus apella)

We introduced two to four unfamiliar animals into three established groups (N = 6–9 per group) of tufted capuchins (Cebus apella).We present findings on the behavioral consequences of introductions as a function of age, sex, and residency status and long-term consequences for health and reproduction. No morbidity from aggression occurred at the time of introductions or during several months following, and reproduction was not compromised. Activity budgets and patterns of social spacing and interaction were little changed following the introductions except for increases in vigilance behavior, especially by newly introduced adult females. Adult females exhibited the strongest and longest-lasting response to changes in group composition. The results indicate that in this species (1) introductions of adult females can be carried out with acceptable risk to the newcomers provided that careful monitoring occurs, so that the onset of severe aggression instigated by resident females toward new females can be avoided, (2) juveniles can be introduced with minimal risk, and (3) adult males can be introduced into groups lacking resident adult males with minimal risk. Capuchins differ in important ways from the better-studied Old World monkeys in their response to introductions of strangers. The differences are instructive with regard to processes supporting species-typical social structure, which is less overtly hierarchical in capuchins than in macaques.     

Pestle use and modification by tufted capuchins (Cebus apella)

We examined the use and modification of pestles by tufted capuchins (Cebus apella). In each of two experiments we presented 18 subjects with an apparatus that held sugarcane along with materials that the animals could use as tools. In Experiment 1 we presented the subjects with sticks, and in Experiment 2 we presented them with sticks, stones, paper towels, and food biscuits. Seven subjects used sticks as pestles to break down fiber to and squeeze sap from sugarcane in Experiment 1. Five of them modified sticks for this purpose. In Experiment 2, 10 animals used pestles and sponges, combined tools, and used pestles to mix together different kinds of food. These results provide further evidence of functional convergence for the use and modification of tools byCebus andPan and are consistent with the view that extractive foraging is associated with the tool-using and toolmaking behavior of primates.     

Transfer index and mediational learning in tufted capuchins (Cebus apella)

The transfer index (TI) is a discrimination reversal paradigm that requires the achievement of a given prereversal criterion of accuracy. The mediational learning (ML) paradigm is a modification of the TI procedure that features the presentation of three different reversal conditions designed to assess whether prereversal learning is based on purely associative processes or mediated by the use of a strategy (win-stay/lose-shift). These two paradigms have been used with apes and several Old World monkey species, proving to be effective tools for the comparison of species on the basis of their transfer abilities and the nature of their learning processes. However, among New World monkeys, only the squirrel monkey has been tested. Capuchin (Cebusspp.) adaptability and their mastery in using tools have led to controversial interpretations of their cognitive and learning skills. We evaluated their mode of learning and the transfer of learning using the TI and the ML paradigms. We tested four tufted capuchins (Cebus apella)in a WGTA using a variety of stimulus object pairs. The results show that they possess rather good transfer abilities and one subject showed an associative learning mode. None of the subjects showed evidence of learning mediated by a win-stay/lose-shift strategy.     

Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella)

The responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella) were investigated. In both species the amount of fear behavior was higher in the presence of the model than during baseline conditions. Unlike the macaques, in the capuchins the frequency of these behaviors decreased across trials. In the two species the amount of explorative and manipulative behaviors and the use of space were also different. Unlike macaques, all capuchins manipulated the objects available in the testing room, and three subjects contacted the apparatus by using objects. Macaques did not show significant preferences for any particular part of the testing room. In both conditions, capuchins used the floor more than macaques did. Further, capuchins increased the use of the floor across experimental trials. Latency to reach the floor was higher in macaques than in capuchins. When on the floor, capuchins spent most of the time close to the snake apparatus. It is proposed that the behavioral differences between capuchins and macaques in the responses to a potential predator indicate that capuchins have a greater propensity to explore and to contact the novel stimulus directly, or by means of objects, than macaques do. These tendencies may lead to the exploitation of novel features in the environment.     

Development of maze navigation by tufted capuchins (Cebus apella)

Theories of spatial navigation hypothesize that animals use vector or topological information to choose routes, often including detours, to move objects or themselves to goals. We assessed adult capuchin monkeys’ (Cebus apella) navigation through 192 virtual two-dimensional mazes that incorporated detour problems. Six monkeys initially were significantly less likely to choose the correct paths when detours were required than when not. Three of the six monkeys repeatedly practiced the 192 mazes to asymptotic mastery; the other three did not practice the mazes again. In a subsequent transfer test, each monkey made correct choices equivalently often on familiar and novel mazes, which suggests that they used general planning skills for maze navigation. Of the three monkeys that practiced the 192 maze-set repeatedly, one efficiently detoured and the other two significantly improved detouring compared to their initial performance. Two monkeys, contrary to their performance when completing the 192 maze-set for the first time, made correct choices at the same rate as chimpanzees. Some evidence suggested that two monkeys used topological information, but utilization of vector information was obvious for all monkeys. Our findings suggest that the boundaries of any individual's navigational abilities are not predicted by species, but depend on experience.     

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.     

Predictors of reproductive success in female white-faced capuchins (Cebus capucinus)

Early investigations into variable reproductive success in nonhuman primates tended to focus on the benefits conferred by high dominance rank. However, the effect of high rank on individual reproductive success has been found to vary both intra- and interspecifically, requiring researchers to expand their investigations to include additional factors. Here we examine the age and rank of the mother, sex of the infant, group size, number of close kin, replacement of group males, and resource availability as possible predictors of female reproductive success in white-faced capuchins (Cebus capucinus) in the Santa Rosa sector of the Area de Conservación Guanacaste, Costa Rica. We examine the length of interbirth intervals (IBI) and infant survivorship as measures of individual reproductive success for the 31 adult females that resided in our three study groups between 1986 and 2007. The greatest predictor of IBI length was whether or not the first infant in the interval survived (number of matrilineal kin and resource availability were also significant predictors); while infant survivorship was most significantly predicted by the occurrence of a turnover in group males in the year following the birth of an infant (infant sex was also a significant factor). Based on these findings, we conclude that male and female reproductive strategies are at odds in this species, with male strategies strongly influencing female reproductive success.     

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.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

Twinning in tufted capuchins (Cebus apella): rate, survivorship, and weight gain

We calculated the rate of twinning across four captive collections of tufted capuchins (Cebus apella) to be 2.4%. This rate contrast with previous reports that twinning in tufted capuchins is rare. Additionally, we present data on the survival and weight gain of twins in this species as compared to singletons. Twins face their greatest risk of mortality on or before the first day of life, when 45% will die compared to 16% of singletons. After the first day of life, twins and singletons demonstrate comparable survival rates. This, in conjunction with the finding that at no time during the first year of life do twins and singletons differ significantly in their weights, suggests that twinning is a viable reproductive form for these animals, especially in the captive setting where nutritional demands are met.     

Hematological and plasma biochemical values for captive tufted capuchin monkeys (Cebus apella)

Hematological and blood biochemical parameters are of great importance in medical and veterinary practice. Unfortunately, normal reference range intervals for hematological and serum biochemical values in the tufted capuchin monkey (Cebus apella) have seldom been reported. The study reported here is based on data from blood samples collected from 44 monkeys over an 8-year period. Male and female data are displayed separately within two age categories: juveniles and adults, and effects for sex and age are examined. Significant differences between males and females are found for erythrocytes, hemoglobin, hematocrit, and α(1) globulin. Significant differences between juveniles and adults are found for neutrophils, calcium, aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase, inorganic phosphorus, glucose, total protein, serum iron, and some serum protein parameters and albumin/globulin ratio. These values are compared with values we previously reported, and their importance in care and well-being of captive tufted capuchin monkeys is discussed.     

Quantification of hair cortisol concentration in common marmosets (Callithrix jacchus) and tufted capuchins (Cebus apella)

Quantifying cortisol concentration in hair is a non‐invasive biomarker of long‐term hypothalamic‐pituitary‐adrenal (HPA) activation, and thus can provide important information on laboratory animal health. Marmosets (Callithrix jacchus) and capuchins (Cebus apella) are New World primates increasingly used in biomedical and neuroscience research, yet published hair cortisol concentrations for these species are limited. Review of the existing published hair cortisol values from marmosets reveals highly discrepant values and the use of variable techniques for hair collection, processing, and cortisol extraction. In this investigation we utilized a well‐established, standardized protocol to extract and quantify cortisol from marmoset (n = 12) and capuchin (n = 4) hair. Shaved hair samples were collected from the upper thigh during scheduled exams and analyzed via methanol extraction and enzyme immunoassay. In marmosets, hair cortisol concentration ranged from 2,710 to 6,267 pg/mg and averaged 4,070 ± 304 pg/mg. In capuchins, hair cortisol concentration ranged from 621 to 2,089 pg/mg and averaged 1,092 ± 338 pg/mg. Hair cortisol concentration was significantly different between marmosets and capuchins, with marmosets having higher concentrations than capuchins. The incorporation of hair cortisol analysis into research protocols provides a non‐invasive measure of HPA axis activity over time, which offers insight into animal health. Utilization of standard protocols across laboratories is essential to obtaining valid measurements and allowing for valuable future cross‐species comparisons.     

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.     

Coated nuts as an enrichment device to elicit tool use in tufted capuchins (Cebus apella)

The present paper describes a simple technique that hardens the shell of nuts and makes the use of a tool to crack them open more compelling. Walnuts were coated with a dough of sawdust and nontoxic white glue in different combinations; they were tested for hardness by using machines normally used to test different kinds of wood. Data on relative hardness for uncoated walnuts and walnuts coated with dough of two different combinations are presented. The coated walnuts were significantly harder to break than the uncoated ones, whereas no significant difference was found when comparing the hardness of two types of coated walnuts. Furthermore, observations on a captive group of tufted capuchins (Cebus apella) are described. The monkeys needed significantly more time to break open the coated walnuts. Early results show that coated walnuts may favor acquistion of tool use skills in a juvenile capuchin.     

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.