Biochemical and hormonal correlates of dominance and social behavior in all-male groups of squirrel monkeys (Saimiri sciureus)

This study examined the relationship between dominance rank and several physiological and behavioral measures in stable, captive, all-male squirrel monkey groups. Four groups, each containing three males, were observed for 12 weeks during the breeding season. Relative dominance ranking among males in each group was based on the direction of agonistic behaviors displayed. For each subject, whole blood serotonin (WBS), plasma testosterone (T), and cortisol (C) were sampled 4 to 6 times over the course of the study. Samples were separated by 1- to 2-week intervals. Each group had a stable linear dominance hierarchy. WBS had small intraanimal variance and was positively related to dominance rank. In contrast, T and C were highly variable within subjects and were unrelated to dominance rank. Among alpha males, concentrations of T and C were positively correlated, and WBS and C were negatively correlated. The effect of dominance rank on the relationship between within-animal fluctuations in WBS, T, and C and behavior was also assessed. In dominant, but not subordinate subjects, intraanimal fluctuations in WBS correlated with agonistic behavior initiated, and fluctuations in C and T correlated with huddling. In beta and gamma males, C was related to agonism received, and in gamma males to food stealing received. Dominance status also affected endocrine response to the stress of capture but not the rate of sneezing. Sneezing was positively correlated with T concentrations irrespective of dominance rank. These results extend the association between WBS and dominance rank previously reported in Old World monkeys to a New World monkey species, support previous suggestions that mean T and C titers are not reflective of dominance rank in well-established groups, and indicate that dominance rank affects adrenocortical response to the stress associated with capture and anesthesia.     

Diurnal variations of androgens in sexually mature male Bolivian squirrel monkeys (Saimiri sciureus) during the breeding season

To assess diurnal fluctuations of serum androgens and cortisol in adult male Bolivian squirrel monkeys, these steroids were measured at predetermined times (0300, 0900, and 2300 hours) during two separate 24-hour periods in the breeding season (January 1983 and late November 1983). A significant diurnal change in serum cortisol was noted, with a nadir of 99.9 ± 11.9 μg/dl (x? ± SEM) at 2300 hours and a peak of 168.9 ± 7.8 μg/dl at 0900 hours. Conversely, a nadir in serum testosterone was noted at 0900 hours (117 ± 26.5 ng/ml) increasing to a peak of 328.5 ± 57.9 ng/ml at 0300 hours. Serum androstenedione and dehydroepiandrosterone followed a pattern similar to testosterone, with a serum androstenedione (176.4 ± 34.9 ng/ml) and dehydroepiandrosterone (11.7 + 1.8 ng/ml) nadir at 0900 hours and a plasma androstenedione (494.5 ± 55.4 ng/ml) and dehydroepiandrosterone (32.5 ± 4.1 ng/ml) peak at 0300 hours. Parallel changes of testosterone, androstenedione, and dehydroepiandrosterone suggest a significant contribution of all three androgens from a common site, the testes. In contrast to old world primates and humans, serum androstenedione levels exceeded serum testosterone levels in this species.     

Prenatal ionizing irradiaton and early postnatal growth of Colombian and Bolivian squirrel monkeys (Saimiri sciureus)

Fetal squirrel monkeys of Bolivian and Colombian origin were exposed to 100 rad cobalt-60 radiation in utero and carried to term by the dams. Body weight, head circumference, crown–rump length, and food intake were measured during the first 28 postnatal days. Significant subspecies differences were noted in both mothers and offspring, the Colombian squirrel monkeys being generally larger than the Bolivians. The irradiated offspring weighed significantly less, had significantly smaller crania, and consumed significantly less food than control animals. A statistically nonsignificant decrement was also evident in the crown–rump length of radiation-treated infants.     

Location effects of social partner on experimental foraging in the squirrel monkey

The effect of social context on experimental foraging in squirrel monkeys (Saimiri sciureus) was investigated. The 12 subjects comprised six pairs in which strong social preference and attraction had been demonstrated during observations of a stable group. Individuals were first trained to discriminate spatially separated rich and poor foraging bins containing 75% and 25% of the food items, respectively, with their partners restrained equidistant from the two bins. The monkeys invested an average of 75.5% of their foraging time in the rich bin. Each individual was then tested with its partner restrained in different locations relative to the bins to determine the effect of partner proximity on foraging patterns. Foraging efficiency at the start of a session was enhanced when the partner was restrained adjacent to the rich bin compared to restraint away from this bin. Over an entire foraging session, however, all conditions providing partner accessibility were similar in yielding enhanced foraging efficiency compared to partner absence. Little time was spent in close physical proximity to the partner under any condition. It is suggested that accessibility of the social partner, rather than close physical proximity, has an important influence on the foraging squirrel monkey. © 1995 Wiley-Liss, Inc.     

Diurnal and annual variation of adrenocortical activity in the squirrel monkey

Diurnal changes in basal cortisol levels and stress reactivity were assessed in male and female squirrel monkeys. Blood samples were collected at four-hour intervals throughout the day and night in the mating and nonmating seasons. Basal cortisol levels in females were similar in both seasons, but males tended to have higher cortisol levels during the mating season, especially at night. For both sexes, cortisol secretion was highest between 0400 and 0800 preceding the onset of the diurnal activity period. Assessment of cortisol responses following brief handling and anesthesia indicated that stress responses were relatively stable across the year, but cortisol increments were slightly higher in the nonmating season. Cortisol levels post-stress were generally related to prior baseline values. Thus, a knowledge of biorhythmic changes in basal hormone levels was important for predicting hormone levels after acute stressors. Males also underwent marked seasonal variation in their basal testosterone levels, which markedly altered the nature of their testosterone responses 30-minutes poststress. © 1995 Wiley-Liss, Inc.     

Maternal recognition of individual infant squirrel monkeys from isolation call playbacks

Responses of six squirrel monkey (Saimiri sciureus) mothers to playback of a single call type, the “isolation peep,” made by their own infants were tested after mothers and infants had been separated for more than a week. The playback tapes were edited from tapes containing mixed vocal material recorded when infants and mothers could see but not touch each other. Mothers showed recognition of their own infants compared to other familiar infants by increases in four measures of proximity to the speaker. These data provide evidence that maternal recognition of infants by means of acoustic cues is possible when the test stimuli consist of examples of a single call type with demonstrated individuality.     

Abnormal behaviors in nursery-reared squirrel monkeys (Saimiri sciureus)

Seventeen squirrel monkeys (Saimiri sciureus), 11 nursery-reared and six mother-reared, were monitored to clarify the type and degree of deviant behaviors that result from rearing this species in the nursery. Two observation periods were used: the first when the subjects averaged 6.7 months of age, the second when they averaged 15.5 months. Thirteen activities involving variations of nonnutritive orality, stereotypic posturing, and agitated behaviors were seen in the nursery-reared subjects, but never in the mother-reared subjects. No consistent gender, subspecies, or age differences were evident. Squirrel monkeys, like chimpanzees and some Old World monkeys, do develop atypical self-directed behaviors when deprived of normal stimulation during early development.     

A study of postnatal appendicular skeletal maturation in captive-born squirrel monkeys (Saimiri boliviensis)

This study is based on a mixed longitudinal radiographic sampling of appendicular bones in 82 captive-born squirrel monkeys (Saimiri boliviensis). All appendicular ossification centers had appeared radiographically by 17 weeks of age, and epiphyseal fusion was complete by 47-53 months of age. No statistically significant differences were found between the sexes in comparisons carried out at birth and at 6 and 8 months of age. Valid sex comparisons could not be made at other ages owing to the small size of the sample. The sequence of appearance of the ossification centers (Spearman correlation coefficient of Saimiri vs. Callithrix = 0.68) shows greater interspecies differences than the sequence of fusion (Saimiri vs. Callithrix = 0.88).     

Sequences and timing of dental eruption in Bolivian captive-born squirrel monkeys (Saimiri sciureus)

Squirrel monkeys, colony-born from Bolivian parents, were studied to establish the sequences and timing of eruption for deciduous and permanent teeth. Infants were born with a naked gingiva, and in only one monkey was di₁ present at birth. The eruption of the lower deciduous teeth preceded their upper counterparts with the exception of di2, dc, and dpm2. No significant differences were found between the right and left quadrants of the mandible and maxilla. No significant sexual differences were found in the age of eruption. By the age of 14 weeks, all deciduous teeth had erupted. The sequence of eruption of the replacement teeth was different from that of milk teeth. The differences lie in the delayed eruption of canine teeth and in the inverted sequence, from the back to the front, of the premolar series. Significant sexual differences were found in total eruption (TE) for PM₃ and I² (P < 0.05) and highly significant differences (P < 0.01) in TE and initial eruption (IE) for C¹, females being more precocious than males. The age at which monkeys completed dental eruption was highly variable, 103–119 weeks for males and 89–112 weeks for females. Differences were found when our results were compared with those of Long and Cooper [1968] for Colombian squirrel monkeys.     

Effect of separation distance on isolation call structure in squirrel monkeys (Saimiri sciureus)

Isolation calls of captive squirrel monkeys were recorded by separating infants from their natal group members and then permitting vocal contact between the “lost” baby and the group at systematically varied distances. Separated infants gave longer calls at greater separation distances from their natal group members, and responding adults and juveniles similarly extended the length of their vocalizations. In the longer variants, a highfrequency element was prolonged, which is considered to be an example of the net advantage of a “frequency window” in the ambient noise of environments.     

Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.     

The influence of behavioral context and social characteristics on the physical aspects of social grooming in rhesus monkeys

The extent to which dominance status and sex can influence the physical act of grooming was examined in two groups of rhesus monkeys. Both the sex and the dominance status of the groomee, but not of the groomer, were found to affect the body sites groomed and the positions assumed by the animals during the grooming bout. Females were groomed more on the back and head and less on the tail, rump, upper leg, and lower arm than males. Females with infants tended to face away from the groomer. Higher-ranking groomees were groomed more on the tail and rump and less on the upper leg and back than lower-ranking groomees. Higher-ranking groomees spent more time lying down during grooming than lower-ranking groomees, while lower-ranking groomees faced away from the groomer more then higher-ranking groomees. The behavioral interactions just prior to and immediately after grooming were also recorded. Although the onset of grooming was preceded by social interactions between the partners, the end of grooming was followed by a complete break in interactions. Particular types of social signals displayed by the groomee just prior to grooming were highly correlated with the grooming of specific body sites. These results suggest that the groomee controls the behavior of the groomer by the social signals it displays and the positions it maintains during the grooming bout. Thus, the grooming act itself may play an important role in the social relationships between group members.     

Age-related hormonal differences in cycling squirrel monkeys (Saimiri boliviensis boliviensis)

This study was planned to evaluate the poor reproductive performance of aged squirrel monkeys in a self-sustaining breeding colony. Two groups of monkeys aged 6–8 years (Group 1), and >12 years (Group 2) were evaluated. During the midbreeding season, daily blood samples were obtained for a period of 35 days from 10 animals in each group. Blood samples were assayed for serum estradiol (E), progesterone (P), and bioassayable luteinizing hormone (bio-LH) concentrations and the data were analyzed by ANOVA (analysis of variance). Bio-LH surges were less frequent in the aged breeders (Group 2). Total P output during periovulatory period (day ?;3 to day + 3) and the total P output during the luteal phases of the estrus cycles were significantly lower in aged squirrel monkeys (Group 2, P < 0.003). Although E peaks occurred less frequently in Group 2, they had higher concentrations as compared to Group 1 (P < 0.003). Cumulative periovulatory and luteal phase E levels did not differ between the two groups. The reduction in P output in aged squirrel monkeys may interfere with proper implantation, thus contributing to the lower pregnancy rate observed in this age group. The decreased frequency of bio-LH surges indicated less frequent ovulations in the aged animals which may further impair reproduction with aging. © 1994 Wiley-Liss, Inc.     

Conditions of failure and recovery of maternal behavior in captive squirrel monkeys (Saimiri)

This paper deals with the functioning and malfunctioning of maternal behavior in relation to external and social conditions. During developmental studies in captive squirrel monkey groups, 49 mother-infant pairs were observed. There were several cases of maternal inadequacy subsequent to (1) postnatal transportation, (2) exaggerated social investigation by immatures,and (3) premature allomothering. Brief mother-infant separations by humans did not yield such failures. One female consistently prevented nursing with at least three of her five viable offspring. Complete or partial failure of maternal behavior did not preclude subsequent recovery and/or adequate allomothering. Dedicated to Prof. Dr. Med. Detlev Ploog on the occasion of his 60th birthday.     

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.     

Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus

This study tested the "challenge hypothesis" and rank-based predictions for temporal steroid production in male tufted capuchin monkeys, Cebus apella. Fecal samples (n = 209) collected from six wild males were analyzed for testosterone and cortisol concentration by enzyme immunoassay. The temporal pattern in male steroid production was compared to female sexual activity and rates of male aggression. The top-ranking adult male did not differ from other adult males in testosterone or cortisol concentration. Mean adult testosterone was significantly higher than mean subadult testosterone throughout the year. There was a clear elevation of testosterone and cortisol in both adult and subadult males during the peak of adult female sexual activity after the birth season. In fact, the magnitude of increase in testosterone was higher than predicted for a species with low male-male aggression. However, there was no difference between nonbreeding baseline testosterone levels during the birth season, and the "breeding" baseline of testosterone in males found during asynchronous female sexual activity. Of all behavioral indices examined, the distribution of female-maintained consortships was the best predictor of mean adult male testosterone concentrations. Although in many species, elevated testosterone coincides with increased male-male aggression, in the present study, the sustained high-magnitude increase in steroids during the peak of adult female sexual activity was associated with a relatively low rate of male-male intragroup aggression.     

In vitro fertilization analysis of squirrel monkey oocytes produced by various follicular induction regimens and the incidence of triploidy

An in vitro fertilization system utilizing squirrel monkeys was used to compare follicle-stimulating hormone, clomiphene citrate and prostaglandin E₁ as follicular induction regimens, analyze culture medium characteristics, and examine the physiological phenomenon of polyspermy. Induction of follicular growth was poor with clomiphene citrate when compared to the control group and increased the incidence of atretic follicles at all levels tested. When prostaglandin E₁ was administered, larger numbers of mature oocytes were recovered at laparoscopy. There was no difference in fertilization rate between the treatment and control groups. Homologous serum was an adequate protein source in TC-199 fertilization medium for squirrel monkey oocytes. Although the rate of triploidy was increased with in vitro fertilization, there was no relationship between sperm concentration and the incidence of polyspermy. These findings demonstrate that the squirrel monkey is a valuable primate system for studies of in vitro fertilization and preimplantation development. © 1993 Wiley-Liss, Inc.     

Endocrine aspects of social instability in the olive baboon (Papio anubis)

The relationships among social status and the cortisol and testosterone stress-response were studied in the non-natal male members of a troop of olive baboons (Papio anubis) before and during a period of social instability. The unstable period was characterized by dominance interactions that were more frequent, more inconsistent, and produced less linear hierarchies than during the stable period. These changes occurred predominantly among the high-ranking males. Such males engaged in coalitions and consortship harassments at a higher rate during the unstable period than during the stable period. Finally, high-ranking males had the highest rates of involvement in and initiation of escalated fighting during the unstable period, in contrast with the stable period. A number of endocrine correlates of instability emerged. During the stable period, high-ranking males (by reproductive criteria) showed an endocrine profile different from that of subordinates. They had the lowest basal cortisol titers, the largest and fastest increases in cortisol titer during stress, and had elevated testosterone titers during stress. None of these attributes was found in high-ranking males during the unstable period. Males during the unstable period had elevated basal cortisol titers, suppressed cortisol responsiveness to stress, and no longer showed elevated testosterone titers during stress. When psychological advantages associated with social status in a stable social environment were lost, endocrine efficiency previously associated with social status was apparently also lost. Further, high-ranking males, who were most aggressive exclusively during the unstable period, had the highest absolute titers of testosterone exclusively during the unstable period. Thus, elevated testosterone and high levels of aggression were unrelated to social status during the period of social stability, but were traits associated with dominant individuals during the unstable period.     

Behavioral and physiological suppression of fertility in subordinate marmoset monkeys

In laboratory groups of common marmosets (Callithrix jacchus jacchus), socially induced reproductive suppression among subordinates and offspring effectively maintained a monogamous breeding system. Male subordinates or male offspring were inhibited or restrained from showing sexual behavior, while similarly placed females could also suffer from complete ovarian failure. In well-established families, a familiarity or inbreeding taboo restricted reproduction among otherwise fertile offspring. However, only one daughter ovulated in any family, and in up to 50% of family groups, all daughters were inhibited from ovulating. This differential effect on daughters may have reflected a qualitative shift in the mother-daughter relationship: the ovulating daughter may have represented the next breeding female and may no longer have regarded the mother as an inhibitory influence. In newly established peer groups of pubertal and postpubertal offspring, one male and female dominated all others in each group and overtly inhibited sexual behavior in subordinates of their own sex. Ovulation was suppressed in all subordinate females because of inadequate gonadotrophin secretion. This was not related to increased secretion of cortisol or prolactin, but may have been related to hypothalamic inhibition of luteinizing hormone-releasing hormone (LHRH) secretion.