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.     

Dietary variability in Cebus apella in extreme habitats: evidence for adaptability

The dietary composition of Cebus apella in two subtropical forest environments of Argentina reflects the seasonal availability of potential food resources. In the marginal areas of the geographical distribution of this species, different resources are used during periods of scarcity. A greater tendency to use leaves in the diet is observed in the northwest (El Rey National Park), where there is greater seasonal variation of fruit availability. In El Rey, where there are few potential resources, the diet is dominated by a few resources, notably bromeliads. Where the resources are more abundant and the availability is more constant throughout the years (Baritú and Iguazú National Parks), the monkeys exhibit a feeding behavior similar to that seen in tropical areas. This ability of the genus Cebus to exploit resources not accessible to other primate species is one of the reasons for its wide geographical distribution and its widespread existence in ecosystems marginally used by primates.     

Facial Displays in Cebus apella

Tufted capuchins are diurnal New World primates whose social interactions involve vocal and visual communication. We aimed to describe their facial displays and assessed the use (in relation to rank and age/sex classes of the sender or the receiver or both) and the social function of the most frequent ones. More specifically, we analyzed the temporal relationship between each facial display and specific classes of behaviors, e.g., play, aggression, performed by the sender and by the receiver (Pre-Post-Event Histogram [PPEH]). We observed 20 captives, belonging to 2 groups, for a total of 320 h. The capuchins displayed relaxed open-mouth, silent bared-teeth, open-mouth threat, lip-smacking, open-mouth silent bared-teeth, scalp lifting, and, rarely, protruded lips. The repertoire and the meanings of the different facial expressions are similar to those described for Catarrhini. In some cases, such as for the silent bared-teeth display, the meaning depends on the age of the sender. Silent bared-teeth is associated with play in juveniles and with submissiveness of the sender to the receiver and affiliative interactions in adults. The finding, and the fact that silent bared-teeth display is used during courtship (Carosi and Visalberghi, 2002), support Preuschoft and van Hooff’s (1995, 1997) power asymmetry hypothesis of motivational emancipation, according to which there is convergence between affiliative and submissive behaviors in species with a high degree of social tolerance.     

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.     

Constitutive heterochromatin polymorphism in Lagothrix lagothricha cana,Cebus apella,and Cebus capucinus

We describe the C-bands in the karyotypes of Lagothrix lagothricha cana, Cebus apella and Cebus capucinus. The C-banding patterns show both a high degree of polymorphism as well as the presence of terminal and interstitial C-bands. Varying amounts of heterochromatin result in dimorphism of some chromosome pairs. The high incidence of chromosome rearrangements found in the Cebidae may be due to the presence of terminal and interstitial C-bands.     

Food competition in a semi-free-ranging Cebus apella group

The competitive regime faced by individuals is fundamental to modelling the evolution of social organization. In this paper, we assess the relative importance of contest and scramble food competition on the social dynamics of a provisioned semi-free-ranging Cebus apella group (n = 18). Individuals competed directly for provisioned and clumped foods. Effects of indirect competition were apparent with individuals foraging in different areas and with increased group dispersion during periods of low food abundance. We suggest that both forms of competition can act simultaneously and to some extent synergistically in their influence on social dynamics; the combination of social and ecological opportunities for competition and how those opportunities are exploited both influence the nature of the relationships within social groups of primates and underlie the evolved social structure.     

Experimental gastric carcinogenesis in Cebus apella nonhuman primates

The evolution of gastric carcinogenesis remains largely unknown. We established two gastric carcinogenesis models in New-World nonhuman primates. In the first model, ACP03 gastric cancer cell line was inoculated in 18 animals. In the second model, we treated 6 animals with N-methyl-nitrosourea (MNU). Animals with gastric cancer were also treated with Canova immunomodulator. Clinical, hematologic, and biochemical, including C-reactive protein, folic acid, and homocysteine, analyses were performed in this study. MYC expression and copy number was also evaluated. We observed that all animals inoculated with ACP03 developed gastric cancer on the 9(th) day though on the 14(th) day presented total tumor remission. In the second model, all animals developed pre-neoplastic lesions and five died of drug intoxication before the development of cancer. The last surviving MNU-treated animal developed intestinal-type gastric adenocarcinoma observed by endoscopy on the 940(th) day. The level of C-reactive protein level and homocysteine concentration increased while the level of folic acid decreased with the presence of tumors in ACP03-inoculated animals and MNU treatment. ACP03 inoculation also led to anemia and leukocytosis. The hematologic and biochemical results corroborate those observed in patients with gastric cancer, supporting that our in vivo models are potentially useful to study this neoplasia. In cell line inoculated animals, we detected MYC immunoreactivity, mRNA overexpression, and amplification, as previously observed in vitro. In MNU-treated animals, mRNA expression and MYC copy number increased during the sequential steps of intestinal-type gastric carcinogenesis and immunoreactivity was only observed in intestinal metaplasia and gastric cancer. Thus, MYC deregulation supports the gastric carcinogenesis process. Canova immunomodulator restored several hematologic measurements and therefore, can be applied during/after chemotherapy to increase the tolerability and duration of anticancer treatments.     

Cognitive processes in Cebus monkeys (Cebus apella) when solving problem-box tasks

Although monkeys are capable of solving problem-box tasks, they were said to perform without 'understanding the value of unlocking' and to use 'kinesthetic control' only [Kohts, 1928]. However, the cognitive processes are much more complex--at least in Cebus monkeys: the problem-solving process was conducted according to the position of the catch in relation to the edge of the door, i.e. our monkey learnt to use visual control. The main characteristics of the monkey's behavior were similar to those exhibited by children. Problem-box tasks proved to be a suitable method for the comparative analysis of cognitive processes in primates.     

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.     

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.     

Postnatal growth allometry of the extremities in Cebus albifrons and Cebus apella: A longitudinal and comparative study

Cebus albifrons and Cebus apella, partially sympatric capuchin monkeys from South America, are known to differ substantially in adult body mass and bodily proportions. C. apella possesses a robust, stocky build in contrast to the more gracile, relatively longer limbed body design of C. albifrons. Average birth weights and adult body lengths of these two congeners, however, are remarkably similar and do not serve to distinguish them. This study examines longitudinal growth rates and patterns of ontogenetic scaling in the extremities (humerus, radius, hand, femur, tibia, foot) in order to document the nature and magnitude of skeletal changes associated with increasing age and body mass. Our data indicate that the growth rates of the six skeletal components of the limbs differ only slightly and somewhat inconsistently between the two species. Body mass, however, increases at a consistently faster rate in C. apella. Relative to body mass, therefore, the extremities of C. albifrons scale much faster than those of C. apella. This implies that at any given postnatal body mass, C. albifrons is longer limbed than C. apella. Conversely, C. apella is heavier than C. albifrons at any given limb length or age. We suggest that such differences in body mass distribution are causally related to differences in locomotor behavior and foraging strategies. Specifically, the relatively long-limbed C. albifrons is probably more cursorial and tends to travel longer distances each day than C. apella. C. apella is a much more deliberate quadruped and is also characterized by especially vigorous and powerful foraging and feeding behaviors. We also compare our results to other (mostly cross-sectional) studies of skeletal growth allometry in nonhuman primates.     

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.     

Multifocal candidiasis in a capuchin monkey (Cebus apella).

Candidiasis involving nasal, pharyngeal, and intestinal mucosal surfaces and a pharyngeal lymph node was demonstrated microscopically in a young adult female capuchin monkey (Cebus apella) experimentally infected with Schistosoma haematobium (Iran strain). Persistent nasal exudation and weight loss characterized the clinical disease preceding the animal's death.     

Esterase D in Cebus apella from the Amazonian region*

Research programs involving the study of genetic variation of proteins have been carried out both in humans and catarrhine primates but rarely in New World species. Considering the great possibilities offered by protein variations as genetic markers in systematic and evolutionary studies in this group of organisms, the authors are specially interested in the investigation of genetic polymorphisms of blood proteins in Amazonian primates. In this paper we describe the electro phoretic patterns of erythrocyte esterases obtained from blood samples of 57 Cebus apella specimens. Blood hemolysates from Cebus display four main set of bands in azo-coupled stained gels. These bands are identified as esterases P, A1, A2 and B by their electro phoretic migration, substrate specificity and eserine reaction. The use of the fluoregenic reagent 4-methylumbelliferyl acetate revealed the presence of a fifth set of enzymes not detected by the azo-coupled staining method. This ser of enzymes, probably a polymorphic genetic system, was named ESD as in humans.     

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.