Cage Design and Forms of Play in Red-Bellied Tamarins,Saguinus labiatus

We investigated the role of cage design in the expression of play in a group of red-bellied tamarins (Saguinus labiatus). For each of the four play behaviors that were measured in this study (wrestle, pounce, grasp, and chase), significant differences in frequency appeared as a function of substrate. When playing on broad, flat, horizontal substrates, the tamarins primarily wrestled with one another. When playing on branches and vines, the tamarins wrestled less but chased and grasped more. Play sequences were less varied in terms of inclusion and order of play behaviors when they occurred on flat, horizontal substrates. To the extent that zoo or laboratory enclosures are outfitted with substrates, whose size and physical orientation are at odds with a species' natural habitat, the validity of play data and the educational value of an exhibit are compromised. © 1992 Wiley-Liss, Inc.     

Sleeping Site Selection by Captive Tamarins (Saguinus labiatus)

We investigated the sleeping site preferences of three captive groups of red-bellied tamarins (Saguinus labiatus), especially as those preferences might relate to protection and safety. The tamarins chose sleeping boxes that offered the most concealment, the greatest distance from the floor, and the greatest cover overhead. They did not, however, avoid sleeping boxes that were attached to the floor via vines. When the tamarins had no choice but to sleep in a box that offered little in the way of concealment, they increased their rates of vigilant scanning. Whereas a number of considerations other than those related to predation pressures must also affect sleeping site choices, we have demonstrated that, under controlled circumstances, these primates choose to sleep in locations in which they are hidden and inaccessible.     

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.     

Karyotype of Saguinus labiatus labiatus (red-bellied marmosets)

The karyotype of Saguinus labiatus labiatus was determined by the Giemsa-banding technique on leukocytes cultured from 10 marmosets. The diploid chromosome number (2n = 46) was the same and the chromosome complement similar to other marmosets of genus Saguinus. Small karyotypic differences were found between S. l. labiatus and white-lipped marmosets (Saguinus fuscicollis) in the size of the X chromosome and in the banding pattern of one pair of metacentric chromosomes. A karyotypic variant was detected in 1 S. l. labiatus, characterized by a diploid chromosome number of 45 with balanced autosomal translocation involving two pairs of acrocentric chromosomes (T 16/19).     

Reproduction of wild-caught marmosets (Saguinus labiatus labiatus) under laboratory conditions.

The reproductive performance of marmosets (Saguinus labiatus labiatus) was evaluated under laboratory conditions. Nineteen of 22 (86%) male-female pairs produced 32 live births during the first 18 months in the laboratory. The reproductive performance and survival rates were comparable to those of other Saguinus species maintained under similar conditions.     

The Perception of Sex-specificity in Long Calls of the Tamarin (Saguinus labiatus labiatus)

Long calls given by red-chested moustached tamarins (Saguinus l. labiatus), typically 1–2 s in duration and made up of individual syllables, reveal distinctive sex-specificity as well as population and individual differences in their acoustic structure. Distributions of male calls and female vocalizations are discrete with regard to two acoustic parameters, i.e. number of syllables and mean inter-syllable intervals. Mean number of syllables produced in a given time is much greater in male than in female calls. I played back synthetic versions of the long calls varying in mean inter-syllable intervals to captive tamarins and found that the sex differences were encoded in a relatively simple acoustic form. The tamarin is able to identify the sex of unfamiliar calling conspecifics by voice alone.     

A case study employing operant conditioning to reduce stress of capture for red-bellied tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

Field Techniques for Monitoring Cotton-Top Tamarins (Saguinus oedipus oedipus) in Colombia

We present reliable field techniques for capturing, anesthetizing, and Iidentifying individual cotton-top tamarins (Saguinus oedipus oedipus). A new technique is presented for radio-tracking small bodied primates. A backpack-style harness was designed to carry a transmitter. This system appears effective in minimizing potential injury and does not appear to interfere with the normal behavior of the animal. © 1993 Wiley-Liss, Inc.     

Visual monitoring of threatening objects by captive tamarins (Saguinus labiatus)

Captive social groups of red-bellied tamarins (Saguinus labiatus) were observed in the presence of threatening, inanimate objects. The tamarins monitored the stimuli over the course of the 20-minute trials by conducting brief, periodic visual checks of the objects. The average number of checks per subject per trial was stable both across trials and between groups, and individual differences in rates varied relatively little around the group means. These data generate the hypothesis that there is a species-typical execution of vigilance in the presence of mildly threatening objects. This execution takes the form of brief visual inspections of the stimulus, usually by one tamarin at a time, at a fairly consistent rate. The discussion of the data takes place in the context of the behavioral ecology of callitrichid species.     

Locale-specific Vocal Behaviour of the Tamarin (Saguinus I. labiatus)

A quantitative acoustic analysis of long calls of red-chested moustached tamarins (Saguinus l. labiatus) was undertaken after capture in the primary forest of Northwestern Bolivia, comparing two populations. Two acoustic parameters are statistically significantly different. Acoustic properties distinguishing individual heterogeneity are quite consistent between the groups and completely different from cues separating population variability. As these two study groups were only 27 km apart when trapped, and as no geographical barriers prevented genetic exchanges between them, we assume populational vocal variability comparable to dialects in birds.     

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.     

The Effect of the Captive Environment on Activity of Captive Cotton-Top Tamarins (Saguinus oedipus)

This study examined captive cotton-top tamarin (Saguinus oedipus) behavior across 3 different exhibits: (a) a rainforest (30.5 m in diameter), where tamarins free-ranged with other species; (b) a caged outdoor exhibit (5 m in diameter); and (c) a caged enclosure, with access indoors (6 × 9m) and outdoors (2.5 × 2.5 m). The study observed tamarins using focal animal scan sampling in 10 min blocks. Scoring was on the percentage of intervals in which they engaged in 12 behaviors. The findings show significant differences in activity, inactivity, and visibility across exhibits and have important implications for reintroduction efforts.     

Susceptibility of tamarin (Saguinus labiatus) red blood cell membrane lipids to oxidative stress: implications for wasting marmoset syndrome

Captive Callitrichids frequently suffer a fatal wasting disease, wasting marmoset syndrome (WMS), of unexplained cause. This paper describes studies on the erythrocytes from animals in a breeding colony of tamarins (Saguinus labiatus), in which deaths from anaemia and wasting were occurring, to seek evidence for biochemical changes which could lead to oxidative damage and premature cell lysis. In only one animal of 33 studied did the red blood cell lipids show an increased susceptibility to oxidative damage. This animal, with some degree of certainty, could be diagnosed as having WMS. It was concluded that evidence for a primary deficiency of antioxidants as a cause of unexplained deaths, or WMS, in the colony could not at present be substantiated.     

Spatiotemporal Interactions Among Three Neighboring Groups of Free-Ranging White-Footed Tamarins (Saguinus leucopus) in Colombia

Successful conservation requires an understanding of animal movement patterns and space use. Such data are hard to obtain, however, when difficult terrain, nocturnal habits, or lack of habituation make direct observation impractical. White-footed tamarins (Saguinus leucopus) are small primates endemic to Colombia that are in danger of extinction due to habitat loss, fragmentation, and the illegal pet trade. Here, we report the results of the first study to use radio-tracking to investigate white-footed tamarin ranging behavior. We recorded the movements of three neighboring tamarin groups simultaneously for 3 month using radio-telemetry. Home range sizes (estimated using both minimum convex polygon and fixed kernel contour methods) were substantially larger than reported in previous studies that did not use remote-tracking. Monte Carlo resampling procedures revealed that home range size differed significantly among the three groups but that the mean daily path length did not. As in other tamarin species, the degree of range overlap between neighboring social groups was high, ranging from 27 to 81%. Using a randomization test, we showed that the observed mean distance between groups was significantly lower than expected by chance for two of the three group dyads. This pattern of intergroup “attraction,” in conjunction with substantial range overlap and high population density, implies that the Bellavista Forest, one of the few remaining habitats of Saguinus leucopus, may be saturated, and promoting habitat restoration should be a priority for the conservation of this species.     

The Effect of Infant Body Mass on Carrier Travel Speed in Cotton-top Tamarins (Saguinus oedipus)

Infant carrying is common in primates and may be the second most costly activity related to reproduction, after lactation. In cooperative breeding groups of callitrichids, all group members carry and care for twin infants. Previous studies have described the costs of infant carrying in terms of body mass loss and reduced locomotor capability. However, infant carrying may also influence travel speed, an important potential cost because slower speed may handicap foraging, energetic budgets, and predator avoidance. We evaluated the impact of infant carrying on the travel speed of 27 adult and 9 subadult cotton-top tamarins (Saguinus oedipus) of both sexes in large outdoor enclosures. We compared carrier speed to speed when not carrying during the 10 weeks after nine births. Subadult tamarins, which have a lower body mass than adults do, moved faster than adults when not carrying. We found no difference between the mean speeds of subadults and adults while carrying. However, the speed of carriers decreased as infant mass increased, and the slope of this negative relationship was more pronounced in subadult carriers. For every 80 g of extra mass load (the body mass of newborn twins), adults reduced their speed by 6 % and subadults by 19 % relative to noncarrying speed. We also observed a reduction in speed while carrying two infants in adult tamarins as carrying time increased. Our results contribute to an understanding of the costs of infant carrying, and serve to emphasize the importance of cooperative breeding systems in coping with these costs.     

Correction to: Phenotypic,Genetic, and Cytogenetic Evidence of Hybridization between Species of Trans-Andean Tamarins (Genus Saguinus)

International Journal of Primatology - This article is intended for inclusion in the Special Issue on Primate Hybridization and Hybrid Zones. It was however published in a separate issue, Volume 39...     

Comparative studies on vertical separation,foraging behavior and traveling mode of saddle-backed tamarins (Saguinus fuscicollis) and red-chested moustached tamarins (Saguinus labiatus) in Northern Bolivia

The author made comparative studies on the ecology of saddle-backed tamarins (Saguinus fuscicollis) and red-chested moustached tamarins (S. labiatus) on the upper Amazon in northern Bolivia. The unit group of both species of monkeys was a family group composed of two to seven individuals, but they often formed polyspecific associations comprising one such family group each. However, both species preferred different layers of forest for foraging insects and traveling.S. fuscicollis mainly utilized the lower layer of the forest and foraged large-sized insects lurking in tree hollows, whereasS. labiatus mainly utilized the middle layer of the forest and foraged small-sized animals on branches. These differences were more clearly noticeable in secondary forest than in primary forest.     

An outbreak of Yersinia pseudotuberculosis infection in a small indoor breeding colony of red-bellied (Saguinus labiatus) tamarins

A spontaneous outbreak of yersiniosis caused by Yersinia pseudotuberculosis serotype IIB occurred in a small indoor breeding colony of red-bellied tamarins (Saguinus labiatus) during the winter of 1981. Of 35 monkeys at risk 6 died of an acute or subacute infection over a period of 23 days. Clinical signs were anorexia, weakness, listlessness and depression. The disease was characterized by focal necrosis of the liver, spleen, mesenteric lymph nodes, ulcerative enteritis, and the presence of colonies of Gram-negative bacilli in the lesions. Y. pseudotuberculosis was isolated from the liver, spleen, mesenteric lymph nodes and kidney but not from the blood, lung or intestine. Contaminated food was believed to be the source of infection.     

Vigilance,vocalizations, and cryptic behavior at retirement in captive groups of red-bellied tamarins (Saguinus labiatus)

Frequent references are made to presumed antipredator adaptations exhibited by callitrichids, but there are very few systematic investigations of these behaviors. One set of untested presumptions stems from observations that callitrichids become especially vigilant and cryptic prior to retirement each evening. This hypothesis was tested in the current study by quantifying the rates of vocalizations and extragroup behavior at various times of the day. Using two groups of captive red-bellied tamarins, it was demonstrated that these primates do become relatively more quiet and more attentive to the nonsocial environment prior to retirement each evening, culminating in virtual silence once the nest box has been entered. While the adaptive significance of these phenomena has not yet been tested, it is likely that the behaviors reduce vulnerability to predation.     

Non-random association of opsin alleles in wild groups of red-bellied tamarins (Saguinus labiatus) and maintenance of the colour vision polymorphism

The remarkable X-linked colour vision polymorphism observed in many New World primates is thought to be maintained by balancing selection. Behavioural tests support a hypothesis of heterozygote advantage, as heterozygous females (with trichromatic vision) exhibit foraging benefits over homozygous females and males (with dichromatic vision) when detecting ripe fruit on a background of leaves. Whilst most studies to date have examined the functional relevance of polymorphic colour vision in the context of foraging behaviour, alternative hypotheses proposed to explain the polymorphism have remained unexplored. In this study we examine colour vision polymorphism, social group composition and breeding success in wild red-bellied tamarins Saguinus labiatus. We find that the association of males and females within tamarin social groups is non-random with respect to colour vision genotype, with identified mating partners having the greatest allelic diversity. The observed distribution of alleles may be driven by inbreeding avoidance and implies an important new mechanism for maintaining colour vision polymorphism. This study also provides the first preliminary evidence that wild trichromatic females may have increased fitness compared with dichromatic counterparts, as measured by breeding success and longevity.