The dynamics of social organization in a population of squirrel monkeys (Saimiri sciureus) in a seminatural environment

A population of about 200 squirrel monkeys (Saimiri sciureus) living in a seminatural environment at the Monkey Jungle in Goulds, Florida, were studied to determine the composition of the population and the basic pattern of its social structure. The social associations of 95 tagged individuals were recorded over a period of three years to determine the basic social organization of the population. The monkeys lived in one group of male juveniles and three female-centered groups with peripheral male subgroups. In spite of the homogeneity of the environment, the groups utilized different foraging strategies which was reflected in differences in the mean weight of adult females. Although females changed subgroup affiliation, they remained within the same large group. Males, however, rarely changed subgroups, but the subgroups frequently changed their group affiliation.     

Social and reproductive behaviors in surrogate-reared squirrel monkeys (Saimiri sciureus).

A colony of 16 surrogate-reared squirrel monkeys was observed for the adequacy of social and reproductive behaviors at maturity. Aside from some self-directed abnormalities centering around nonnutritive orality, this group was behaviorally normal in spite of having no contacts with mother-reared, older conspecifics. Half (N=5) of the females gave birth, with four infants viable. One infant has remained with the colony and is thriving. The other three remained with the group for as long as 42 days before death or removal. Maternal care appeared adequate. Mean estimated conception age for females was 35 months, and the mean impregnation age for males was estimated to be 42 months.     

Mutual dependencies between vocal and visual signals of squirrel monkeys

Visually recognizable social signals and structural call components, which had been demonstrated to be of social relevance within their own communication channel in previous experiments (disregarding or experimentally excluding other ones), were treated together, and their inter-dependencies analyzed when they were performed simultaneously in spontaneous behavior sequences of pairs of adult squirrel monkeys. It was found that: (1) all call classes were uttered within periods when either genital display or “triumph gesture” were shown; (2) production rates of particular vocal classes significantly deviated from no-display periods; (3) degree and direction of deviations (more/less frequent) were quite specific for both vocal and nonvocal classes (Figs. 1a & 1b); (4) differences depended also on which animal actually displayed (the vocalizing one, the other one, or both; Fig. 3); and (5) differences found for single animals when they played different roles in the experimental situation were smaller than those found between individuals, which could be related to dominance status (Table 2). The possibility of mutual modification of signals of different modalities and perspectives for future work are discussed.     

Social interactions of monkeys reared in a nuclear family environment versus monkeys reared with mothers and peers

Four-year-old laboratory-born rhesus monkeys that had been reared in a nuclear family social environment consisting of mothers, fathers, siblings, peers, and other adults of both sexes were permitted to interact in various combinations with equal-aged monkeys that had been reared in an environment consisting of only mothers and peers. It was found that in most interaction sessions nuclear family subjects exhibited significantly higher levels of dominance and activity behaviors and significantly lower levels of submissive and passive behaviors than the mother-peer-reared subjects. These differences were not evident when subjects were tested within their own rearing groups. The significance of the results with respect to previous and future studies of social development in differential social environments is discussed.This research was supported by grant No. MH-11894 from the National Institute of Mental Health to the University of Wisconsin Primate Laboratory, by the Grant Foundation, and by grant No. RR-0167 from the National Institutes of Health to the University of Wisconsin Primate Research Center.     

Social context as a structuring mechanism in captive groups of squirrel monkeys (Saimiri sciureus)

Various classes of individuals were removed from three captive groups of squirrel monkeys and effects measured on the frequencies of nonagonistic interactions of the remaining individuals. Results indicated that there are regularities in the effects of certain classes of dyadic relationships on others which may be considered species-typical structuring mechanisms ofSaimiri social groups and which account for in consistencies which have appeared between experimentally identified social preferences of adults of this species and their actual behavior in social groups. A tentative process model ofSaimiri social structure and its seasonally changing character is presented and implications of this kind of analytical model for studies of evolution and adaptation are briefly discussed.     

Social hierarchy under different criteria in groups of squirrel monkeys,Saimiri sciureus

Under different criteria the individual members of groups of squirrel monkeys show different social capacities. The ranking of the subjects was much the same for Restraining and Genital display. The hierarchies for Approaching and Following fitted well with each other, showing few similarities with the above two. Location of individual ranks for Withdrawing tended to be the opposite to that of Approaching and Following. Restraining and Genital display showed quasi-linear hierarchies, with males on top and females at the bottom of them. For Approaching, Following, Withdrawing, and Genital inspection the results varied from quasi-linear structure to circular or even unisexual arrangement. As a rule the animals behaved towards partners close in rank to themselves. Several individual roles could be isolated: An alpha male role, directing Restraining and Genital display to all other partners more frequently than any of them towards him, basing his ability more in adequate distribution of total performance among social partners than in high total frequency; an omega male role under the same criteria, whose function would be to connect with the hierarchy of females and a scapegoat role, a very passive female receiving all kinds of attention from most subjects.     

Vigilance during play in squirrel monkeys

Play by young squirrel monkeys (Saimiri boliviensis) may put them and other troop members at risk for predation because youngsters are noisy, separated from adults, and not vigilant when at play. In a study using separated groups of adults and 1-year-old juveniles caged outdoors, we found that adult female squirrel monkeys become more vigilant during periods of spontaneous play among juveniles. This behavioral response could be obtained with auditory cues (play vocalizations) alone. Five times as much vigilance activity was directed toward an area from which threat or disturbance was likely to come as was directed toward the juveniles themselves. These results suggest both an adaptive, compensatory increase in adult vigilance during play and a function for play vocalizations. Additional functions for play vocalizations remain to be investigated.     

Social organization and social behavior in two subspecies of squirrel monkeys (Saimiri sciureus).

Social organization and social behavior were examined in two subspecies of squirrel monkeys which differ markedly in the degree of sexual dimorphism. The Bolivian squirrel monkeys, the subspecies with greater sexual dimorphism, manifested a sexually segregated form of social organization, while the social organization of the Guyanese monkeys was sexually integrated. Dominance relationships were found to reflect these patterns of sexual segregation or integration; in the Bolivian social groups separate linear dominance hierarchies were established within each sex while the Guyanese monkeys established a single linear hierarchy which included both males and females. Relationships between males and females in the two subspecies appear to be regulated by two distinct mechanisms, dominance in the Guyanese monkeys and sexual segregation in the Bolivians.     

Ultrasound-guided follicular aspiration in squirrel monkeys

The objective of this study was to test whether ultrasound-guided oocyte retrieval is an effective mechanism for collecting oocytes in squirrel monkeys. Although ultrasound-guided follicular aspiration has been described in Old World primates, oocyte retrieval in New World primates is typically performed via laparoscopy or laparotomy. However, these procedures, especially the first, can be invasive. Ultrasound has been used for pregnancy monitoring in multiple species of primates including Saimiri spp. Transabdominal ultrasound as a diagnostic tool is non-invasive. Transabdominal ultrasound was utilized to visualize ovarian follicles during aspiration under light anesthesia. This procedure resulted in collection of a total of 29 oocytes from six animals with minimal post-procedural pain. Manipulated animals were returned to the social group the same day.     

Exchange of phospholipids between low and high density lipoproteins of squirrel monkeys

Ultracentrifugal analysis of the plasma of squirrel monkeys at various times after the injection of [Me-(14)C]choline revealed the specific activities of lecithin in both high (HDL) and low (LDL) density lipoproteins to be similar. This was also true for sphingomyelin. The exchange of phospholipids in vitro was studied by incubating unlabeled plasma with labeled LDL and HDL isolated 40 hr after the injection of [Me-(14)C]choline. Recentrifugation of plasma immediately after the addition of either (14)C-labeled LDL or HDL demonstrated that significant exchanges of both lecithin and sphingomyelin had occurred. In further studies, (14)C-labeled LDL or HDL were incubated with plasma and the low density lipoproteins were rapidly isolated by precipitation with heparin-Mn(2+). Complete equilibration of lecithin and sphingomyelin between LDL and HDL was attained after 4 and 5 hr, respectively. The fractional exchange rates for lecithin and sphingomyelin of LDL to HDL were 0.60 hr(-1) and 0.45 hr(-1). Corresponding values for HDL to LDL were 0.51 hr(-1) and 0.53 hr(-1). Inhibition of plasma lecithin:cholesterol acyltransferase reduced the exchange of sphingomyelin but had no effect on lecithin exchange. The rates of exchange of four lecithin subfractions of different unsaturation between LDL and HDL were the same.     

Reciprocity and partner preference in grooming of female blue monkeys

Grooming among adult and older juvenile females in a wild group of blue monkeys (Cercopithecus mitis stuhlmanni) is analyzed and related to agonistic behavior. Both grooming and agonistic behavior were less frequent than would be expected in baboon and macaque groups. Fair shares of grooming were given and taken, both within and between interactions, in amost dyads, and all females were seen to groom with at least half the others. The reciprovity of grooming was its most outstanding feature. There was no evidence that grooming was preferentially directed at kin. Frequent grooming partnerships fell into two clusters, one of which ranked higher than the other. We suggest that grooming throughout the group helps to establish a coherent team of females which effectively, defends its territory in daily encounters at the boundaries with neighboring groups.     

Encephalitis induced by a canine distemper virus in squirrel monkeys

Intracerebral inoculation with canine distemper virus (CDV) caused acute neurological signs of viral encephalitis in squirrel monkeys. Electroencephalogram revealed an abnormal sharp wave and seizure discharges resembling those of epilepsy. There was parenchymal inflammation, perivascular cuffs, neuronal degeneration, and glial reactions. Virus antigen was detected immunohistologically in the neurons and ependymal cells. Thus, CDV infection in squirrel monkeys provides an animal model for viral encephalitis and epilepsy.     

Social context affects how rhesus monkeys explore their environment

This study reports on social modulation of exploratory behavior and response to novelty by members of a captive rhesus monkey colony. The group was trained to split in half, with one subgroup composed of dominant members only, the other of subordinates. The animals were then presented the same initially novel stimuli (i.e., sand-filled metal boxes containing hidden food items) in two social contexts differing in hierarchical composition. In a combined context, all group members (i.e., both subgroups together) were simultaneously presented the stimuli. In a split context, only members of the top or bottom half of the group (i.e., each subgroup in turn) was independently presented the stimuli. Subordinates responded similarly to dominant animals in the combined context but differently in the split context, where they were far more hesitant. Rank-related differences were evident in the way animals used their home compound and in their approach and responsiveness toward the stimuli. These findings show that social context influences how animals explore novel situations, possibly reflecting different social roles or status effects on the perception of social structure. Also, despite the complexity of primate social relationships, the separation technique produced no permanent or adverse effects on the social integrity of the group. This study shows that manipulating the social environment through separation training can be a powerful tool for assessing contextual influences on behavior. Am. J. Primatol. 44:205–214, 1998. © 1998 Wiley-Liss, Inc.     

Cerebral beta-amyloid angiopathy in aged squirrel monkeys

Cerebral beta-amyloid angiopathy (CAA) is an age-related disorder of the brain vasculature that is involved in up to 20% of non-traumatic cerebral hemorrhage in humans. CAA is a risk factor for cognitive decline, and may exacerbate the dementia of Alzheimer's disease. Progress in discovering the cause and potential therapies for this disorder has been hindered by the paucity of animal models, particularly models of idiopathic CAA. The squirrel monkey (Saimiri spp) develops significant CAA in the natural course of aging. To evaluate the suitability of Saimiri as a model of human CAA, we studied the distribution and composition of Abeta subtypes in CAA and parenchymal (senile plaque) deposits in the brains of aged squirrel monkeys, as well as the relationship between vascular beta-amyloid deposition and comorbid vasculopathies that occur in aged humans. Our findings show that: 1) CAA consists ultrastructurally of classical amyloid fibrils and is the principal type of cerebral beta-amyloidosis in squirrel monkeys; 2) The two primary isoforms of Abeta (Abeta40 and Abeta42) coexist in most microvascular and parenchymal lesions of Saimiri, although Abeta40 tends to predominate in larger arterioles; 3) CAA and parenchymal plaques overlap to a considerable degree in most affected brain areas, and are distributed symmetrically in the two hemispheres; 4) Both CAA and plaques are particularly abundant in rostral regions and comparatively sparse in the occipital lobe; 5) Capillaries are especially vulnerable to CAA in squirrel monkeys; and 6) When CAA is severe, it is associated with a small, but significant, increase in other vasculopathies, including microhemorrhage, fibrinoid extravasation and focal gliosis. These findings, in the context of genetic, vascular and immunologic similarities between squirrel monkeys and humans, support the squirrel monkey as a biologically advantageous model for studying the basic biology of idiopathic, age-related CAA, and for testing emerging therapies for human beta-amyloidoses such as Alzheimer's disease.     

Fasting hyperbilirubinemia in normal squirrel monkeys.

The plasma of Bolivian squirrel monkeys, unlike that of Brazilian squirrel monkeys, is markedly yellow due to unconjugated hyperbilirubinemia after an overnight fast. The fasting hyperbilirubinemia in Bolivian squirrel monkeys is likely due to two mechanisms. First, a twofold increase in the bilirubin turnover/production rate occurs during a 24-hour fast. A second mechanism is the decreased hepatic conjugation potential for bilirubin due to the presence of a higher bilirubin UDP-glucuronosyltransferase UDPGAKm and a lower Vm; this results in higher steady-state plasma and hepatic bilirubin levels during a fast when hepatic UDP-glucuronic acid levels are low. The Bolivian squirrel monkey provides an excellent animal model for human Gilbert's syndrome type I in which to study rate-limiting mechanisms in the movement of bilirubin from plasma to bile.