The social behavior of a marmoset (Saguinus fuscicollis) group II: Behavior patterns and social interaction

The behavioral patterns and social interaction of a marmoset (Saguinus fuscicollis) group in a semi-naturalistic environment were observed for 14 months. The analysis showed that, of the 32 behavior patterns observed, the 10 most frequent accounted for over 97 per cent of the total behavior. One pattern, sit and look, accounted for 44 per cent of the total behavior. The two most frequent social behavior patterns, grooming and social play, were concentrated in different parts of the group. The focal point of grooming was the adult female; social play was characteristic of younger animals 4–20 months of age. These results were compared with other studies of marmosets and with primate studies on grooming and social play.     

The social behavior of a marmoset (Saguinus fuscicollis) group III. Spatial analysis of social structure.

The social behavior, and particularly the spacing patterns, of a marmoset (Saguinus fuscicollis) group in a semi-naturalistic enclosure were observed for 14 months. Data analysis revealed various changes as the group grew in size from four to eventually six members. Weekly mean distances between the adult pair supported a spatial measure for estrus for the female. Group dispersion, mean squared distance between all possible pairs, seemed to vary with the age composition of the group. Factor analysis of location correlation matrices by 4-week blocks resulted in age-related subgroupings. Each of the adult pair formed an independent subgroup except for behavioral estrus and early infant care periods when they formed one subgroup. The offspring, initially attached to the adults, gradually moved into juvenile/subadult subgroups. Increasing spatial independence was shown as an animal approached adulthood at 24 months of age.     

Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae)

We present data on aspects of the behavioral ecology of a free- ranging group of Saguinus fuscicollis weddelliat a site in Brazilian Amazonia where a second callitrichid, Callithrix emiliae,is syntopic. Diet, activity patterns, and ranging behavior are broadly similar to those of S. fuscicollisfrom sites in Bolivia, Brazil, and Perú, though significant seasonal changes include an extreme and atypical form of ranging behavior in which they foraged in central-place fashion around a source of exudate—Parkia pendula. S. f. weddelliwas active at relatively low levels in the forest both in absolute terms and relative to C.emiliae, which appears to be an important factor in their niche partitioning. Association between the two species appeared to be less systematic overall than those observed between S. fuscicollisand congeners at other sites, though this may be partly a result of observation conditions. During the period of central-place foraging, the two species exhibited a high degree of association. Other characteristics of the behavior of S. f. weddelliat the study site include the frequent use of tree holes as sleeping sites.     

Infanticide in a group of wild saddle-back tamarins, Saguinus fuscicollis

An infanticide was observed in a group of wild saddle-back tamarins, Saguinus fuscicollis. The newborn singleton was killed by its mother after it had fallen from the carrier several times. This infanticide may represent a case of parental manipulation: the mother terminated investment in an offspring that probably had a low chance of survival. Also, stress associated with the simultaneous pregnancy of another adult female in the group may have played a role.     

Congenital anomalies in two neonatal tamarins (Saguinus oedipus and Saguinus fuscicollis)

Congenital anomalies were seen at necropsy of two neonatal tamarins. The defects included achondroplastic-like dwarfism, polydactyly and syndactyly in a Saguinus oedipus, and scoliosis and uterus didelphys in a S. fuscicollis. Both infants were the offspring of incestuous matings between twin siblings.     

Vigilance in Single- and Mixed-Species Groups of Tamarins (Saguinus labiatus and Saguinus fuscicollis)

By forming larger sizes of groups, individuals benefit from a decrease in vigilance, but the collective vigilance of the group as a whole is not compromised. We examined whether this group size effect is apparent in mixed-species groups of red-bellied tamarins (S. labiatus) and saddleback tamarins (S. fuscicollis) which form stable and permanent associations in the wild. We studied general vigilance and responses to hidden threatening stimuli in five captive groups of each species, while they were housed in single- and mixed-species groups. For vigilance, the individual rate was lower in the larger mixed-species groups than in the smaller single-species groups. In addition, the amount of time when at least one individual was vigilant was higher in mixed-species groups. This suggests that the tamarins alter their vigilance behavior in the presence of the other species. In response to hidden threats, both species performed brief vigilance checks and frequencies of checking did not differ in single- and mixed-species groups. However, both species had a significant reduction in the mean duration per check, and there was a reduced total amount of time spent vigilance checking in the mixed-species groups compared to the single-species groups, demonstrating the group size effect. Overall the mixed-species groups had a higher number and mean duration of checking than the smaller single-species groups. Given that the two species share a common set of predators, and respond to each other's alarm calls, these findings provide strong evidence that individuals of both tamarin species may be able to benefit from forming mixed-species groups via improved vigilance and monitoring of threats.     

Parental care and infant development in a family group of captive Sichuan golden monkeys (Rhinopithecus roxellanae): First 20 days

A male Sichuan golden monkey (Rhinopithecus roxellanae) was born on July 24, 1986 to an adult pair on loan from the Chinese government. Physical and behavioral development of the infant, as well as the behavior of the parents, were recorded for the first 20 days of the infant's life. (On Day 21 the trio was returned to the Chongqing Zoo in the People's Republic of China.) The infant pelage was dark gray at birth but soon began changing to the orange-gold color typical of the adults. Forty hours of behavioral data were collected using a combination of scan sampling and all occurrences of selected behaviors techniques. The infant pushed against his mother and pulled toward objects in the enclosure beginning at 4 days of age. Time spent in these behaviors increased steadily and on Day 15 the infant broke contact with his mother for the first time. Mother-infant contact appeared to be maintained by both individuals mutually up to the infant's 10th day of the life. The percentage of time that the infant spent actively embracing his mother began to decline after that while the female continued to spend the majority of her time embracing the infant. During the first few days following the birth, the male always initiated and maintained proximity to the female and the infant. This “vigilant” behavior had declined somewhat by the end of the study.     

Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus)

The involvement of parents and siblings in infant care in similarly composed groups of common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) was compared during the infants' first 8 weeks of life. The results indicate an earlier infant independence in C. jacchus than in S. oedipus due primarily to a more frequent rejection of carried infants in C. jacchus. There was no species difference in extent of maternal involvment in carrying infants. However, S. oedipus fathers carried infants significantly more often during weeks 5–8 than did C. jacchus fathers. Siblings were generally more involved in infant care at an earlier infant age in C. jacchus than in S. oedipus.     

Rank orders of arising,eating, and retiring in a family group of tamarins (Saguinus fuscicollis)

A family group of tenS. fuscicollis, housed in a greenhouse and subjected to natural variations in day length, was observed for a period of three months. All animals ordinarily slept together in the same hutch box. The order in which the various animals emerged in the morning was almost the precise inverse of the order in which they retired at night. Each of these orders was quite reliable and was related in nonlinear fashion to age—the ranks of the youngest offspring being the closest to those of the parents. Time of emergence and eating in the morning consistently preceded sunrise by about 30 min and was initiated by the oldest offspring; retiring was much more variable and was led by the parents.     

Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis)

The effects of different social living conditions on estrogen excretion and on the ovarian cycle of saddle back tamarins were investigated. Urinary estrogens were monitored as indices of ovarian cyclicity in groups of adult females living under the following experimental conditions: (1) five parous females, each living with an adult castrated male (in one of the females plasma estradiol and progesterone were also measured); (2) five adult daughters living with their families. Each daughter was then removed from her family and paired with a vasectomized male. After pairing, scent marks collected from the family were introduced daily to one of the daughters and her mate. Scent exposure was then discontinued and hormone excretion measured for several weeks. The remaining four daughters were not exposed to family scent. The females living with castrated males showed urinary estrogen cycles of an average length of 17.5 ± 1.0 days. The plasma estrogen cycle was of the same length. The females studied under condition 2 showed low, noncycling estrogen levels while living in their families. They responded to pairing with an increase in the level of urinary estrogens, and four out of five showed regular estrogen cyclicity. The fifth female exposed to family scent marks after pairing also showed an increase in urinary estrogens. However, as long as scent transfer was maintained, no cycle was observed. Estrogen excretion increased again, and cyclicity commenced when scent transfer was discontinued. It is concluded that ovarian estrogen production is suppressed and cyclicity does not occur as long as daughters live in their families. Release from suppression and perhaps stimulation by the male cause a rapid increase in estrogen levels and the onset of cyclicity. Chemical stimuli produced by the family, perhaps particularly by the mother, may be involved in reproductive suppression.     

Social facilitation of agonistic responses to strangers in pairs of saddle back tamarins (Saguinus fuscicollis)

The effect of the presence of a familiar social partner on the interactions of saddle back tamarins with unfamiliar conspecifics was studied. Fifteen adult male-female pairs, of which six were composed of a castrated male and an intact female, served as subjects. All subject pairs were given two social encounters during which both mates met a strange male and two encounters during which they met a strange female. In addition, all subjects were given four encounters during which they met the same strangers while their own pair mates were absent. As a group, the subjects showed higher intensities of injurious aggression and of agonistic displays when they met strangers in the presence of their own pair mates. Females and castrated males, as subgroups, showed significant increases in most agonistic responses when they met strangers in the presence of their pair mates. Intact males, however, did not.     

Field observation of snake-mobbing in a group of saddle-back tamarins, Saguinus fuscicollis nigrifrons

At the Rio Blanco in Northeastern Peru a group of 6 saddle-back tamarins was observed to mob two Corallus enydris snakes which were hanging from a liana. These and other observations of snake-mobbing demonstrate that callitricids exhibit a special behaviour against potential predators, which is very similar to the mobbing displays of birds and other mammals. It is suggested that the adaptive significance of snake-mobbing in tamarins lies in the cultural transmission of information about potential predators.     

The benefits of helpers: Effects of group and litter size on infant care in tamarins (Saguinus oedipus)

The Callitrichidae (marmosets and tamarins) typically give birth to twins, and infant care is shared by all group members. The potential benefits to callitrichids of having helpers were investigated in a study of 21 captive cotton-top tamarin (Saguinus oedipus) infants, living in groups with two to 12 older members. Time carried and suckled and amount of food received from other family members were recorded for each infant during the first 12 weeks of life. The results showed that infants in larger groups were carried more and received more food than those in smaller groups. Twin infants in larger families were less likely to be on the same carrier. Singleton infants were carried more than twins but did not receive more food. On average, individual caretakers in larger groups carried less and shared less food with infants than those in smaller groups. When parental contributions to care were analyzed, no effects of group size were found on mothers' contributions to carrying or food sharing, but fathers in larger groups both carried infants less and shared less food with them. There appear to be several benefits of a communal rearing system to cotton-top tamarins. 1) Infants may receive more care in larger families, thus increasing their chances of survival. 2) The burden of care is spread over several animals, reducing the costs to a given individual. 3) The parents, particularly fathers, may benefit most from reducing the costs of investing in the present litter and increasing their ability to invest in future litters.     

Proteins: biologically relevant components of the scent marks of a primate (Saguinus fuscicollis)

We report here the first documentation that proteins contributeto the scent communication system in a primate. Data presentedhere indicate that high molecular weight compounds which arenot airborne are required for perception of the full attractivenessof the scent. Scent marks from the saddle-back tamarin, a SouthAmerican primate, contain a number of water-soluble proteins.Gel electrophoresis documents that the major protein (66 kD)is found in urine, and a second protein (18 kD) comes from thegland secretions. The 18 kD protein produces two distinct bands(14 kD and 4 kD) under reducing conditions. Concurrent behavioralstudies demonstrate that removal of proteins by enzymatic degradationdoes not alter the ability of the tamarins to discriminate betweenscents from different donor types. However, subtle changes insensory quality occur when the proteins have been degraded.In particular, tamarins do discriminate material in which theproteins have been digested from material in which the proteinsare intact. This observation suggests that proteins are a componentof what constitutes the scent image. In addition, they may serveas carriers and/or reservoirs for more volatile ligands thatencode some of the communicatory messages contained in the material.     

Composition and Proposed Nutritional Importance of Exudates Eaten by Saddleback (Saguinus fuscicollis) and Mustached (Saguinus mystax) Tamarins

I provide the first comprehensive data on the composition and mineral content of exudates eaten by saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax) and assess Garber's (1984; 1993) hypotheses on the potential nutritional importance of exudates in the diet of tamarins. In accordance with his initial findings, nutritional analyses show that the gums consumed are relatively high in calcium and may serve to balance a diet otherwise low in this mineral and high in phosphorus. However, the data on the seasonal variation in the amount consumed do not support the hypothesis that exudates are of particular nutritional importance during the later stages of gestation or lactation for saddleback or mustached tamarins.     

Sexual and social behavior of adult saddle-back tamarins (Saguinus fuscicollis), castrated as neonates

The behavior of four adult males castrated as neonates was compared with that of three neonatally sham-castrated males and two untreated males serving as controls. Two males castrated as sexually experienced adults served as additional controls. All males lived in permanent male-female pairs. The interactions of neonatally castrated, sham-castrated, and intact control males with strange conspecifics were tested in a situation analogous to territorial defense. In addition, the interactions of all males with their female pair mates were tested. Neonatally castrated males showed less injurious aggression against strangers and interacted with them less frequently than control males. There were significant differences between both groups of males in some of the agonistic behaviors recorded, but not in all. In pair tests, neonatally castrated males failed to show any coordinated male copulatory behavior but control males did. Males castrated as adults showed rates of mounting and thrusting similar to those of intact controls. Neonatally castrated males tended to interact with their females on a lower level than neonatally sham-castrated and untreated control males. How ever, most differences between both groups in the levels of pair mate interactions were not statistically significant. It is concluded that castration during neonatal life prevents the display of male copulatory behavior in adulthood and selectively affects the display of a number of other behaviors in adulthood. It is not possible at this point to decide whether these results are due to hormonal deficiencies on an organizational or activational level or both. However, data from studies currently in progress suggest that organizational processes might be responsible for part of the effect.