Sociophysiology of squirrel monkeys

Primate sociophysiology is an emerging discipline concerned with understanding the proximate mechanisms that contribute to the generation and maintenance of species-typical social systems. Studies of squirrel monkeys illustrate that sociophysiological processes are more varied than is commonly assumed with respect to both the effective social dimensions that influence physiological function and the nature of concomitant physiological effects. For adult squirrel monkeys, a major consequence of social stimulation is altered regulation of pituitary-adrenal, pituitary-gonadal, and autonomic function. In females, socially-induced physiological changes appear to be independent of specific interindividual relationships with other adults, whereas in males, many sociophysiological effects can be understood only when specific relational attributes are considered. In all instances, adult relationships are associated with distinctly different sociophysiological profiles than have been found for the mother-infant relationship and do not conform to the stress/buffering model within which they are often interpreted.     

Studies of heart disease and failure in aged female squirrel monkeys (Saimiri sp.)

Lesions consistent with heart failure were found in 23 of 88 adult squirrel monkeys that died between 1995 and 1999 at the Squirrel Monkey Breeding and Research Resource (SMBRR). This provided a rationale for a study surveying aged animals in the SMBRR for normal cardiac characteristics, using echocardiography (ECHO) and electro-cardiogram. In the pilot study, ECHO and electrocardiography were performed on 59 healthy female squirrel monkeys aged 10 years or older and 39 five-year-old monkeys. Parameters were heart rate, P-wave duration and amplitude, and PR, QRS, and QT intervals (electrocardiography), and ejection fraction. Two animals with cardiomyopathy were identified and received similar testing. Advanced-study animals had the same measurements, plus left ventricular internal diameter-systole (LVIDs) and -diastole (LVIDd), left atrial diameter-diastole (LADd) and aortic root diameter-diastole (AoRDd) by use of ECHO. Significant differences were found between groups in LADd, and P-wave and QRS interval durations. In a clinical context, these differences were not considered to be substantial. Normal aged female squirrel monkeys had significant increases in heart dimension and longer P- and QRS-wave durations than did monkeys of a five-year-old control group, although the increases were not considered clinically relevant. This study documents myocardial dynamics in healthy saimiri and those with cardiomyopathy.     

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.     

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.     

Cross-modal representation of human caretakers in squirrel monkeys

We tested whether squirrel monkeys have cross-modal representations of their human caretakers with a 0-delay symbolic matching-to-sample procedure. We first trained the monkeys to match photographs of two of their caretakers. After reaching criterion, they were exposed to two test sessions. In these sessions 32 all-reinforced test trials were interspersed among the training trials. In the test trials, a voice, either matching (congruent condition) or mismatching (incongruent condition) with the sample photographs, was played back after the sample stimulus disappeared. The monkeys' matching accuracies in the incongruent condition were lower than in the match condition. Post hoc analyses revealed that the presentation of the primary caretaker's voice interfered with performance in test trials where the secondary caretaker's face was presented (incongruent condition). This suggests that our subjects recalled their primary caretaker's representation upon hearing the appropriate voice.     

Maternal discrimination of infant vocalizations in squirrel monkeys

Responses of mother squirrel monkeys to vocalizations of their own and other infants were examined to determine whether mothers could discriminate their infants on the basis of auditory cues. Thirty mothers, whose infants ranged in age from one to seven months were tested in three conditions in which their own infant, a different infant, and no infant served as the stimulus. Mothers were tested in an enclosed alleyway with opaque end panels behind which stimuli were placed. The quantity and quality of maternal responses clearly differed in the three conditions and indicated that mothers recognized their own infants. Differences in maternal vocalizations were the most pronounced. All but one type of vocalization increased in the own-infant condition; the exception, a high-pitched shrill, decreased. Mothers also spent more time near the stimulus and were more active when tested with their own infants.     

Insect-catching behavior in socially inexperienced infant squirrel monkeys

Insects are an essential component of squirrel monkey natural food. Eight of ten socially inexperienced infant squirrel monkeys, during their 2nd and 3rd month of age, directed their attention to living insects or film presentations of moving insects. They attempted to catch them with gradually improving success, and on at least two occasions consumed them. For comparison, group-living squirrel monkeys begin to eat solid food around their 2nd month of age, continuing with some nursing until about 11 or 13 months, and were only at this age seen to successfully catch and eat insects. Thus, as infant squirrel monkeys proved to be able to catch and eat insects before their first experience with conspecifics, an innate basis for this behavior can be assumed.     

Reproductive synchronization in squirrel monkeys (Saimiri)

Groups of squirrel monkeys (Saimiri) that are exposed to certain seasonal environmental stimuli experience a yearly reproductive cycle with discrete mating and birth seasons. Seasonal rainfall or some rainfall induced seasonal changes (such as changes in vegetation or insect fauna) appear to be responsible for timing theSaimiri reproductive cycle. Animals of both sexes show significant physiological and behavioral changes during the yearly cycle. Whether the environmental timing factors affect both the males and the females equally, or affect only one sex directly and the other sex indirectly through social communication is not clear. Three mechanisms by which the reproductive activity of both males and females could be synchronized are presented, and data from a laboratory study and a field study relevant to each mechanism are presented. Several social interaction patterns frequently observed in the field study suggest that (1) male sexual activity may excite female sexual activity through male penile display and/or other stereotyped interactions and/or (2) female sexual activity may excite male sexual activity through pheromone and/or other communication channels.     

Individuality and stability of isolation peeps in squirrel monkeys

Isolation peeps (IP's) made by captive squirrel monkeys (Saimiri sciureus) of both the Gothic and Roman type have been analysed by spectrographic and statistical methods designed to quantify the degree of individuality found in utterances from single individuals. Clustering analysis confirmed that in both groups of monkeys individually distinct combinations of acoustic features characterize the IP and that such unique combinations persist over periods of several years. Differences between the Gothic and Roman form of the IP were found in more aspects of acoustic structure than had previously been known. The evidence suggests that information about the identity of the vocalizer is contained in the the IP.     

Androgen resistance in squirrel monkeys (Saimiri spp.)

The goal of this study was to understand the basis for high androgen levels in squirrel monkeys (Saimiri spp.). Mass spectrometry was used to analyze serum testosterone, androstenedione, and dihydrotestosterone of male squirrel monkeys during the nonbreeding (n = 7) and breeding (n = 10) seasons. All hormone levels were elevated compared with those of humans, even during the nonbreeding season; the highest levels occurred during the breeding season. The ratio of testosterone to dihydrotestosterone in squirrel monkeys is high during the breeding season compared to man. Squirrel monkeys may have high testosterone to compensate for inefficient metabolism to dihydrotestosterone. We also investigated whether squirrel monkeys have high androgens to compensate for low-activity androgen receptors (AR). The response to dihydrotestosterone in squirrel monkey cells transfected with AR and AR-responsive reporter plasmids was 4-fold, compared with 28-fold in human cells. This result was not due to overexpression of cellular FKBP51, which causes glucocorticoid and progestin resistance in squirrel monkeys, because overexpression of FKBP51 had no effect on dihydrotestosterone-stimulated reporter activity in a human fibroblast cell line. To test whether the inherently low levels of FKBP52 in squirrel monkeys contribute to androgen insensitivity, squirrel monkey cells were transfected with an AR expression plasmid, an AR-responsive reporter plasmid, and a plasmid expressing FKBP52. Expression of FKBP52 decreased the EC50 or increased the maximal response to dihydrotestosterone. Therefore, the high androgen levels in squirrel monkeys likely compensate for their relatively low 5 alpha-reductase activity during the breeding season and AR insensitivity resulting from low cellular levels of FKBP52.     

Malignant uterine mesotheliomas in squirrel monkeys following diethylstilbestrol administration

10 adult female squirrel monkeys were implanted subcutaneously with 4 60 mg pellets of diethylstilbestrol (DES); 4 animals were implanted with cholesterol pellets to serve as controls. Animals were killed at 5, 9, 11, and 14 months after insertion of pellets. All animals implanted with DES had evidence of extreme estrogenic stimulation, including marked edema of the labia, heavy vaginal cornification, and enlargement of the uterine corpus. There were several stages of uterine lesions, in general in proportion to the duration of treatment. The less advanced lesions were restricted to hyperplasia and hyperthrophy of the serosal cells. In more advanced lesions the myometrium was infiltrated; in the most advanced cases there was invasion of the endometrium. The 7 most advanced uterine tumors were classified as malignant mesotheliomas. Cholesterol-treated controls did not have any significant lesions. These observations indicate that DES is carcinogenic in the squirrel monkey, as it has been demonstrated to be in other lower mammalian species.     

Responses of mother squirrel monkeys to dead infants

The responses of mother squirrel monkeys to infants were examined by testing the mothers with bodies of their own and other infants. Mothers whose infants were stillborn or died at one day of age showed strong and equivalent maternal responses to all the bodies with which they were presented, while those whose infants died after two weeks of age responded mainly to the body of their own infant. These results suggest that the female squirrel monkey becomes more selective in responding to the body of a dead infant with the passage of time after parturition. The female's post-parturient condition appears to be the prime cause for changes in her responsiveness, although other factors related to the infant's growth and development might also be important.Supported by Grant HD 04905 from the National Institute of Child Health and Human Development.     

Food-storing behavior in captive squirrel monkeys (Saimiri sciureus)

Observations of food-storing in caged squirrel monkeys are described. Frequencies of storage and attempted retrievals increased with the introduction of novel objects. The type of storage site, its location and defense, all indicate hiding of food or favored objects to avoid stealing attempts rather than food or object play behavior.     

Reconciliation in captive Guyanese squirrel monkeys (Saimiri sciureus)

The tendency for agonistic interaction to increase the probability of friendly interaction between social partners has been demonstrated across a range of Old World primates. While research on such post-conflict behavior proceeds into an hypothesis-testing phase, new comparative information must accumulate to provide full phylogenetic perspective on primate social behavior. Data from New World and prosimian primates are yet extremely limited. We studied captive squirrel monkeys (Saimiri sciureus) via post-conflict (PC) and matched control (MC) observations and analyzed results using both the PC-MC and time-rule methods. Former opponents maintaining affiliative relationships soon engaged in friendly interaction following large proportions of agonistic interactions, whereas non-affiliated individuals, including virtually all male-female pairs, reconciled conflicts rarely. Close-proximity approaching and huddling contact constituted the principal modes of post-conflict amicability. Agonistic interactions of relatively high intensity were most likely to be reconciled and most likely to be reconciled via physical contact. High vulnerability of Saimiri to predation may have favored this species' strong inclination to reconcile soon after agonistic interaction. Research on free-living populations of this and other primate species is needed to illuminate similarities and differences across taxa.