Intimate social behavior in infant interactions in Cebus apella

The development and individual stability of three intimate social behaviors (Lipsmacking, Carrying Attempts, and Facial Inspection) were examined for 43 group-housed Cebus apella infants from birth to 2 years of age. Occurrence of these behaviors was scored from 10-min videotape samples recorded three times a week over that time. Frequency of Lipsmacking and Carrying Attempts by adult males, adult females, and juveniles were all highest in early months and decreased to low levels by the end of the first year. Facial Inspection of partners by infants, in contrast, first began at 3-4 months and increased over time, at least to adult males and juveniles. Correlational analyses indicated stable individual differences in these interactions with infants and outlined a relationship between these intimate behaviors and more general social patterns reported previously for these animals. Results suggest that adult males may play a special role in affording juveniles opportunities for social learning of foraging and manipulative skills.     

Chromosome studies of Cebus apella: The standard karyotype of Cebus apella paraguayanus,Fischer, 1829

Chromosome studies were performed on 40 specimens identified as Cebus apella paraguayanus, Fischer, 1829, which had been wild-caught in Santa Catalina (Republic of Paraguay). Elongated chromosome spreads obtained from lymphocyte cultures were sequentially stained with different techniques, and a constant pattern of 382 bands was identified in all specimens. A standard karyotype based on the measurements of the total chromosome length and the G-Q banding pattern is proposed.     

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.     

Substrate optimization in nut cracking by capuchin monkeys (Cebus apella)

We conducted an experiment to examine the effect of substrate on the nut-cracking behavior of a group of semicaptive capuchin monkeys. We wanted to determine whether tufted capuchin monkeys were selective in choosing the substrate on which they pound nuts, and whether the choice of substrate affected the outcome. Eight adult females and eight juveniles were provided with nuts in the outdoor facility. We found that 1) all adult females and three young capuchins succeeded in cracking nuts; 2) they preferred the hardest substrates (concrete and stone); 3) there is a link between the substrate and the amount of time needed to crack a nut; 4) most young capuchins used various substrates, some of which were inadequate, in a haphazard manner; and 5) there are different forms of nut cracking. We conclude that adult capuchins choose the hardest substrates, and that these substrates support efficient cracking.     

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 × 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. Am. J. Primatol. 44:147–153, 1998. © 1998 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.     

Intraspecific chromosome variation in Cebus apella (cebidae,platyrrhini): The chromosomes of the yellow breasted capuchin Cebus apella xanthosternos wied, 1820

Chromosome studies in six wild-caught specimens of Cebus apella xanthosternos showed a distinctive chromosome pair number 11 that made it possible to distinguish this subspecies from other Cebus apella. The characteristic chromosome pair had intercalar heterochromatin unlike the “standard” chromosome type of Cebus apella and other species of the same genus, in which this chromosome pair shows a large, terminal, heterochromatic block. A comparison at the chromosomal level between different Cebus apella populations suggests that chromosome 11 in Cebus apella xanthosternos is a derived chromosome that has probably become fixed in this subspecies, either by selection or by drift in a small isolated population.     

Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks

In Experiment 1, three capuchin monkeys (Cebus apella) were exposed to a mirror in their home cage for 3 days and then given food treats for touching orange marks located on the surface of an experimental chamber. Following training, a mirror was added to the chamber to see if the monkeys would use it to guide non-reinforced contacts with an orange mark on their foreheads that was only visible as a mirror reflection (mark test). Two monkeys touched the head-mark more often with the mirror present than absent, but no mark touches were emitted while looking at the mirror. In Experiment 2, the monkeys were rewarded for touching orange marks on their bodies that were directly visible, followed by another head-mark test. Again, two monkeys touched the mark more often with the mirror present than absent, but these contacts were not emitted while looking at the mirror. Since facing the mirror while mark touching was not required for reinforcement during training, Experiment 3 further tested the possibility that increased mark touching in the presence of the mirror during Experiments 1 and 2 was the result of a memorial process. For this, a final, novel mark test was conducted using an orange mark on the neck that was only visible as a reflection (Experiment 3). No monkeys passed this test. These are the first mark tests given to capuchin monkeys. The results are consistent with the finding that no monkey species is capable of spontaneous mirror self-recognition. The implications of sequential training and mark testing for comparative evaluations of mirror self-recognition capacity are discussed.     

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. Am. J. Primatol. 48:49–68, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

Pharmacokinetics and pharmacodynamics of interferon beta 1a in Cebus apella

Background  Recombinant human interferon (hIFNβ) is indicated for the treatment of multiple sclerosis. Its effect presents species restriction, thus lacking biological activity on most mammals. Although there have been previous studies of the pharmacology of INFβ in Old World primates, no data exists on New World primates. Therefore, we explored its effect on Cebus apella , a New World monkey, describing the pharmacology of this molecule when injected by subcutaneous route in this species.
Methods  Safety, pharmacokinetics and pharmacodynamics of IFNβ were evaluated in nine Cebus apella individuals.
Results  A single subcutaneous injection of 12 × 10⁶ IU of hIFNβ1a resulted in a median AUC_(0–48) (area under the curve) of 14.82 ng/ml, a C _max (maximum plasma concentrations) of 1.51 ng/ml and a T _max (time to achieve maximum plasma concentrations) of 3 h. IFNβ was biologically active as demonstrated by an increase in neopterin levels. There were no safety concerns.
Conclusions  New World non-human primates are a suitable animal model for the study of IFNβ pharmacology.     

Cytologic, hormonal, and ultrasonographic correlates of the menstrual cycle of the New World monkey Cebus apella

Few reports on the reproductive physiology of Cebus apella have been published. In this study we characterized menstrual cycle events by means of vaginal cytology, ultrasonography (US), and hormonal measurements in serum during three consecutive cycles in 10 females, and assessed the probability that ovulation would occur in the same ovary in consecutive cycles in 18 females. The lengths and phases of the cycles were determined according to vaginal cytology. Taking the first day of endometrial bleeding as the first day of the cycle, the mean cycle length +/- SEM was 19.5+/-0.4 days, with follicular and luteal phases lasting 8.2+/-0.2 and 11.3+/-0.4 days, respectively. The follicular phase included menstruation and the periovulatory period, which was characterized by the presence of a large number of superficial eosinophilic cells in the vaginal smear. The myometrium, endometrium, and ovaries were clearly distinguished on US examination. During each menstrual cycle a single follicle was recruited at random from either ovary. The follicle grew from 3 mm to a maximum diameter of 8-9 mm over the course of 8 days, in association with increasing estradiol (E(2)) serum levels (from 489+/-41 to 1600+/-92 pmol/L). At ovulation, the mean diameter of the dominant follicle usually decreased by >20%, 1 day after the maximum E(2) level was reached. Ovulation was associated with an abrupt fall in E(2), a decreased number of eosinophilic cells, the presence of leukocytes and intermediate cells in the vaginal smear, and a progressive increase in progesterone (P) levels that reached a maximum of 892+/-65 nmol/L on days 3-6 of the luteal phase. The menstrual cycle of Cebus apella differs in several temporal and quantitative aspects from that in humans and Old World primates, but it exhibits the same correlations between ovarian endocrine and morphologic parameters.     

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.     

Blood biochemical indicators in young and adult Cebus apella of both sexes

BACKGROUND: A frequent drawback in physiology of non-human primates is that normal values for a variety of indicators (haematological, biochemical and others) are scant. METHODS: We report here the blood values in a series of 92 healthy Cebus apella (divided by sex, age and pregnancy status). Health check-ups indicated that animals were healthy for the month prior to and after the sampling. Dietary intake was estimated on the basis of two semi-balance studies. RESULTS: Values of haematological indicators, serum LDH activity, micronutrient indicators (serum copper, iron and serum ceruloplasmin concentrations, Zn-Cu-superoxide dismutase activity in erythrocytes) agreed with previous results and provide some values that were not available. Activities of liver enzymes were lower than some previously reported. CONCLUSIONS: These results provide valuable information that help understanding the physiology of C. apella.     

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.     

Social and menstrual cycle phase influences on the behavior of group-housed Cebus apella

This study examined sexual and other social behavior in relation to menstrual cycle phase in four mixed-sex social groups of Cebus apella. Groups consisted of two adult males and either six or nine adult females. Menstrual cycles of high (rank 1–2) and low (rank 3–7) dominance-rank females from each group were monitored via vaginal swabs, and correlated with data collected from ongoing behavioral observations. Only cycles bounded by positive detection of menstrual blood were included in this analysis (n = 15 females, 182 cycles; mean ± s.d., cycle length = 20.8 ± 1.2 days). Rates of copulation and female solicitation of males varied significantly with cycle phase, with highest rates at midcycle. While total rates of solicitation and copulation did not vary with female dominance rank, copulation rates with the dominant male were significantly greater for high ranking females than for low ranking ones. Variance observed in affiliative and agonistic behaviors, including those with males, was attributable to female rank rather than cycle phase. Females and males were also observed attempting to interfere with copulations of lower ranking same-sex individuals. Although further study, particularly of wild populations, is needed, these results indicate that female-female reproductive competition should be included as a component of the capuchin breeding system. As in other primate species, both social and hormone-related factors influence the sexual behavior of Cebus apella. © 1995 Wiley-Liss, Inc.     

Body measurements, hematology, and serum chemistry values of the adult Cebus apella monkey

Body measurements, hematology, and serum chemistry values were studied in 40 captured male and female Cebus apella monkeys. Some significant dimorphism with male predominance was found. Significant differences were also found for hemoglobin and red cell volume between males and females. Differential white blood cell counts indicated a marked predominance of lymphocytes and high values of gamma globulin in both sexes.     

Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella)

Numerous studies investigating behavioral lateralization in capuchins have been published. Although some research groups have reported a population-level hand preference, other researchers have argued that capuchins do not show hand preference at the population level. As task complexity influences the expression of handedness in other primate species, the purpose of this study was to collect hand preference data across a variety of high- and low-level tasks to evaluate how task complexity influences the expression of hand preference in capuchins. We tested eleven captive brown capuchin monkeys (Cebus apella) to determine if they show consistent hand preferences across multiple high- and low-level tasks. Capuchins were expected to display high intertask consistency across the high-level tasks but not the low-level tasks. Although most individuals showed significant hand preferences for each task, only two of the high-level tasks that involved similar hand motions were significantly positively correlated, indicating consistency of hand preference across these tasks only. None of the tasks elicited a group-level hand preference. High-level tasks elicited a greater strength of hand preference than did low-level tasks. No sex differences were found for the direction or strength of hand preference for any task. These results contribute to the growing database of primate laterality and provide additional evidence that capuchins do not display group-level hand preferences.