Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator‐specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive‐born and reared cotton‐top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton‐top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black‐faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator‐naïve cotton‐top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low‐frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive‐reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies. Am. J. Primatol. 70:707–710, 2008. © 2008 Wiley‐Liss, Inc.     

Can Auditory Playback Condition Predator Mobbing in Captive-reared <Emphasis Type="Italic">Saguinus oedipus</Emphasis>?

Captive reintroductions often suffer high mortality, with predation as one source. Many species learn about predators; thus training captive-born animals to recognize predators may increase survivorship. We adapted variants of methods developed for birds to attempt to condition monkeys to mob a predator. Captive-reared cotton-top tamarins (Saguinus oedipus) did not differentiate between a snake and a rat, confirming previous research that naïve cotton-top tamarins do not fear snakes. Tamarins then viewed a living snake during playback of mobbing calls. In posttests, tamarins did not mob the snake. We then eliminated the pretest to avoid potential habituation and placed a stillborn tamarin with the snake in an attempt to heighten arousal. In posttests, tamarins again did not mob the snake, although they did increase their rates of calls, indicating mild arousal. Overall, none of 8 groups of cotton-top tamarins learned to mob a predator. Potential reasons for failure include conditioning multiple subjects at once and the lack of an experienced demonstrator. Observing a demonstrator was not necessary for birds to acquire mobbing, but may be necessary for tamarins.     

Cultural transmission of snake-mobbing in free-ranging Hanuman langurs

A focal troop of free-ranging Hanuman langurs (Presbytis entellus) living in an open scrub forest around Jodhpur was observed mobbing poisonous snakes on two different occasions during field observations of about 4,109 h. These observations of snake-mobbing demonstrate that langurs exhibit a special behaviour against 'potentially dangerous animals' which is similar to the mobbing displays of birds, and of other primates. It is suggested that the adaptive significance of snake-mobbing among langurs lies in the 'cultural transmission' of this information. These observations further support the 'kin-selection' model.     

Predation risk and the interspecific association of two Brazilian Atlantic forest primates in Cabruca agroforest

Forming interspecific associations is one of many strategies adopted by primates in order to avoid predation. In addition to improved predator detection and avoidance, benefits of interspecific associations relate to improved foraging efficiency. In this study we tested these two hypotheses explaining associations between the endangered golden-headed lion tamarin, Leontopithecus chrysomelas and the sympatric Wied's marmoset, Callithrix kuhlii. We estimated predation risk by recording the number of encounters between lion tamarins and potential predators in cabruca agroforest (shaded cacao plantation) and in mosaic forest (a mix of cabruca, primary and secondary forest). To evaluate if the association between the two species was related to foraging benefits we recorded the number of associations between the two species when the lion tamarins were eating and when they were not eating. To test if the association occurred to improve predator detection and avoidance, we evaluated if associations between the species were more frequent in areas with higher predation risk and during the part of the day when predation risk is higher. We also compared the number of associations 3 months before birth events and 3 months after, when the lion tamarins are more susceptible to predation. Predation risk, mainly by raptors, was significantly higher in cabruca than in mosaic forest (0.17 and 0.05 encounters with predators per hour of observation, respectively). Associations were significantly more frequent after birth events and during the part of the day when predation risk was also higher (5-6 am until noon). We did not observe any direct evidence of foraging-related advantages of interspecific associations for the lion tamarins. The tamarins did not associate more when they were foraging. Our findings suggest that lion tamarins are more exposed to predation in cabruca than in mosaic forest and associations between lion tamarins and Wied's marmosets are related to predation avoidance.     

Vigilance and social organization in two species of primates

Animals that live in groups may accrue anti-predator benefits by virtue of their association with other individuals. While a number of factors (e.g. habitat quality, group geometry, dominance rank) have been shown to affect the relationship between group living and individual rates of visual vigilance, sociality and vigilance have not been studied specifically in terms of the two competing demands they impose upon an individual's visual time. Two captive groups each of tamarins, Saguinus labiatus, and squirrel monkeys, Saimiri sciureus, were used in three related experiments to determine whether they looked at the social or non-social environment while they engated in a simulated foraging task. The tamarins, whose social behaviour is quite pacific and cooperative relative to the more hierarchical squirrel monkeys, looked at the non-social environment when they visually interrupted their foraging. Squirrel monkeys, however, looked more often at group mates. Detection of predators is probably more likely when an individual directs its attention not to conspecifics, but to the environment. Hence, social organizations in which individuals must pay social attention in order to monitor threats and avoid aggression may reduce individual rates of vigilance for predators. Failure to consider various targets of attention may well overestimate vigilance for predators by including other sorts of attentional phenomena in the measurement of vigilance.     

Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru

The sleeping habits of moustached tamarins, Saguinus mystax , and saddle-back tamarins, Saguinus fuscicollis , were studied in northeastern Peru. Five types of sleeping sites were distinguished: 1) Jessenia bataua palms; 2) tree hollows; 3) dense tangles of vegetation; 4) crotches; 5) open horizontal branches. Both tamarin species used Jesseniu-palms most frequently. Tree hollows ranked second in the saddle-back tamarins, but were never used by moustached tamarins. Sleeping sites of moustached tamarins were located significantly higher than those of saddle-back tamarins. Jessenia -palms used by moustached tamarins were significantly higher than palms from a random transect sample, but this was not the case for Jessenia -palms used by saddle-back tamarins. For both species, concealment seems to be more important than height above ground. The maximum number of subsequent nights spent in the same sleeping site was two in moustached tamarins and six in saddle-back tamarins. The two tamarin species did not compete for sleeping sites. While the general pattern of sleeping site selection conforms to hypotheses predicting safety from predators as a major factor, differences between the two tamarin species reflect general niche differences between them. Most sleeping sites are located in exclusively used parts of the home range. Moustached tamarins generally use sleeping sites that are close to the last feeding site of the afternoon. The distance between simultaneously used sleeping sites of moustached and saddle-back tamarins are generally close together, which helps to minimize time spent out of interspecific association.     

Reactions of wild tamarins,Saguinus mystax andSaguinus fuscicollis to avian predators

During a field study in northeastern Peru, the reactions of a group ofSaguinus mystax on Padre Isla and of a mixed-species troop ofS. mystax andSaguinus fuscicollis at the Río Blanco to raptorial and other birds were observed. Alarms that are specific to flying stimuli were elicited by birds of prey, but other birds that do not represent a threat to the tamarins also caused alarm calls. Alarm events (i.e., instances when one or more alarm calls were given) were observed at rates of 0.3/hr (Padre Isla) and 0.5/hr (Río Blanco). Rates of alarm events significantly increased after the birth of an infant in the Padre Isla group and after the attack of an ornate hawk-eagle (Spizaetus ornatus) on the Río Blanco group. Reactions to alarming stimuli/alarm calls ranged from looking up to falling down from trees. The modification of the tamarins' behavior by the potential presence of aerial predators indicates that raptors represent an important predatory threat to tamarins.     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

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.     

Golden lion tamarin sleeping-site use and pre-retirement behavior during intense predation

Sleeping sites, their patterns of use, and cryptic pre-retirement behavior mitigate predation risk at sleeping sites and could influence prey fitness. We evaluated sleeping-site usage for 10 groups of golden lion tamarins (GLTs) from a population that recently suffered a substantial decline due to predation at sleeping sites. We recorded the average number of nights that groups spent at their different sleeping sites to determine whether patterns of sleeping-site use were influenced by predation risk, as measured by the rate of encounters with predators, or the availability of suitable sleeping sites, as measured by the size of a group's home range and amount of mature forest within their home range. In addition, we measured travel speed to sleeping sites and compared this speed with that recorded at other times of day. GLT groups spent more nights on average at each of their sleeping sites compared to other callitrichid species for which data are available. Predation risk and habitat characteristics were not significant predictors of how many times groups used each of their different sleeping sites. Groups significantly increased their travel speed just before entering the sleeping site. Rapid locomotion to secure tree cavities may help GLTs avoid crepuscular and nocturnal predators; however, we speculate that this strategy failed numerous GLTs in our study population during the previous decade because they used sleeping sites that were accessible to predators.     

Trypanosoma cruzi infection in Leontopithecus rosalia at the Reserva Biológica de Poco das Antas, Rio de Janeiro, Brazil

Wild golden lion tamarins (Leontopithecus rosalia) - endangered primates that are native to the Brazilian Atlantic coastal forest - were surveyed for the presence of Trypanosoma cruzi with the use of Giemsa-stained blood smears, hemocultures and an indirect immunofluorescence assay (IFAT). Positive IFAT with titers ranging from 1:20 to 1:1280 were observed in 52% of the 118 wild tamarins examined and the parasite was isolated from 38 tamarins. No patent parasitemia was observed among the tamarins from which T. cruzi was isolated. Serum conversion and positive hemoculture was observed for three animals that had yielded negative results some months earlier, which indicates that T. cruzi is actively transmitted among tamarins. In contrast to observations with other sylvatic isolates, those from the tamarins were significantly more virulent and most of them produced mortality in experimentally infected Swiss mice. Some variation in the kDNA restriction profiles among the isolates was observed. Electrophoresis with GPI, G6PDH, IDH, MDH and ME enzymes showed a Z2 profile.     

The effects of social status on food-associated calling behaviour in captive cotton-top tamarins

We examined the effects of social environment on food-asociated calling of cotton-top tamarins, Saguinus oedipus, in two experiments. In experiment 1, we compared the food-associated calling behaviour of six juvenile tamarins living in their natal groups with their calling behaviour 9 months after being removed from family groups and paired. In experiment 2, we studied food-associated calling behaviour of nine cotton-top tamarins immediately before and after removal from their natal groups and pairing. The tamarins underwent three separate developmental processes in their calling behaviour. Animals removed from their natal groups showed an immediate reduction in vocalizations other than food-associated calls (C and D chirps). The development of precise adult forms of C and D chirps was more gradual and was a function of time since removal from their natal group rather than time since pairing. Finally, the postremoval tamarins persisted in applying C chirps to nonfood objects and showed no correlation between C-chirp rate and food preference, which is typical of immature tamarins. We conclude that social status plays an important role in the development of adult forms and usage of food-associated calls. Copyright 1999 The Association for the Study of Animal Behaviour.     

Factors Affecting Group Spread within Wild Mixed-Species Troops of Saddleback and Mustached Tamarins

We examined group spread and interindividual spacing within wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Mustached tamarin groups were spread over larger areas than those of saddleback tamarins. Group size and behavior affected group spread and interspecific proximity: larger groups of both species were dispersed over greater areas, and the larger troop had the lowest degree of interspecific proximity. Behavior also affected group spread and interspecific proximity: when traveling individuals were spread over a larger area, and the distance between heterospecifics was greater than when stationary. We examined spatial proximity using data on the distance from nearest neighbor. Overall, distance to nearest neighbor was not affected by group size. Based on specific behaviors, foraging saddleback tamarins were significantly nearer conspecifics than to mustached tamarins. Tamarins have polymorphic color vision, and trichromats—having 3 types of visual pigment—versus dichromatic individuals—with two types of pigment—may be better at perceiving yellow or russet colored predators and conspecifics than their dichromatic counterparts are. Color vision status affected spatial positioning, with vigilant trichromats being further from their neighbors than their dichromatic conspecifics were. We discuss the findings with respect to the ecology of the species. Specifically, interspecific differences in group spread and spatial proximity are related to differences in the supports used, and the effect of troop size on interspecific proximity is related to increased resource competition. The finding that trichromats are further from their neighbors represents the first example of a behavioral correlate of color vision ability in a wild species with polymorphic color vision, and is explained through the perception of predation risk.     

Focal ulcerative ileocolitis with terminal thrombocytopenic purpura in juvenile cotton top tamarins (Saguinus oedipus)

A newly recognized syndrome characterized by an acute focal ulcerative ileocolitis, anemia and thrombocytopenic purpura in five juvenile cotton-top tamarins is described. The presentation and morphology of this syndrome is distinct from any other reported gastrointestinal disease reported in tamarins. Traditional etiologies such as viruses, ingested toxins, Campylobacter, Salmonella and Yersinia and Clostridium difficile are not considered likely etiologic agents. Nontraditional etiologies such as anaerobes or pathologic strains of Escherichia coli are now being considered. This syndrome is of potential significance to ongoing research into the etiology of idiopathic tamarin colitis.     

Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia)

Seventeen territorial groups of wild golden lion tamarins were monitored for periods of 10–76 months. Immigration into established groups was rare (0.48 immigrating individuals per group per year) and occurred mostly in the context of replacement of breeding individuals. Nonreplacement immigration events usually occurred in conjunction with some other change in group composition (e.g., an emigration or another immigration). Aggression by resident tamarins toward potential immigrants appeared to be the proximate factor limiting movement into groups. Most such aggression was intrasexual, but potential female immigrants were sometimes chased by male as well as female residents. Immigration was highly male biased (85% of individuals). Factors possibly contributing to this bias were inheritance of breeding positions by adult daughters (reducing female and increasing male immigration opportunities), ability of males but not females to join groups already containing a same-sex breeding individual, and the fact that potential female immigrants appeared to face some intersexual as well as intrasexual aggression. Male and female roles in the maintenance of a monogynous mating system are considered in light of these results. Contrasts with data from intruder studies on captive golden lion tamarins [French & Inglett, Animal Behaviour 37:487–497, 1989] are discussed. © 1996 Wiley-Liss, Inc.     

Birth seasonality in cotton-top tamarins (saguinus oedipus) despite constant food supply and body weight

Goldizen et al. (1988) reported that wild saddle-back tamarins (Saguinus fuscicollis, Callitrichidae) show birth seasonality that is correlated with food supply and body weight. They suggested a sequence of ultimate causality in which shortage of food leads to reduced body weight which leads to timing of weaning and lactation when resources are more abundant. Cotton-top tamarins in captivity show birth seasonality despite constant food supply and body weight. Although natural availability of fruit and insects (which are key foods for tamarins) is related to rainfall, birth seasonality and body weight in captive cotton-top tamarins are unrelated to rainfall. The most likely proximate mechanism for seasonality of births in tamarins is photo-period, given existing data on populations living in natural and artificial lighting.     

Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus)

We investigated cooperative problem solving in unrelated pairs of the cooperatively breeding cottontop tamarin, Saguinus oedipus, to assess the cognitive basis of cooperative behaviour in this species and to compare abilities with other apes and monkeys. A transparent apparatus was used that required extension of two handles at opposite ends of the apparatus for access to rewards. Resistance was applied to both handles so that two tamarins had to act simultaneously in order to receive rewards. In contrast to several previous studies of cooperation, both tamarins received rewards as a result of simultaneous pulling. The results from two experiments indicated that the cottontop tamarins (1) had a much higher success rate and efficiency of pulling than many of the other species previously studied, (2) adjusted pulling behaviour to the presence or absence of a partner, and (3) spontaneously developed sustained pulling techniques to solve the task. These findings suggest that cottontop tamarins understand the role of the partner in this cooperative task, a cognitive ability widely ascribed only to great apes. The cooperative social system of tamarins, the intuitive design of the apparatus, and the provision of rewards to both participants may explain the performance of the tamarins.     

Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: Evidence from a thirteen-year study of a marked population

We monitored a population of four to seven groups of individually marked saddle-back tamarins (Saguinus fuscicollis; Callitrichidae) at the Cocha Cashu Biological Station in Peru's Manu National Park every year from 1979 through 1992. In this paper we use data on life histories, group compositions, group formations, and dispersal patterns collected during these 13 years to examine the reproductive strategies of males and females. Group compositions and mating patterns were quite variable in this population, with both monogamy and cooperative polyandry common. In polyandrous groups, two males shared a female's copulations and cooperatively cared for her young. Although most groups contained a single breeding female, we recorded four cases in which secondary females successfully reared young. Most young females appeared to wait in their natal groups for the first opportunity to fill a primary breeding position in their own or a neighboring group. Females that acquired primary breeding positions maintained those positions for a mean of 3 years. No female was observed to transfer between groups a second time. Variation in female lifetime reproductive success was high. Half of the females marked as juveniles never bred; the other half produced an average of 3.5 young. A paucity of female breeding opportunities may explain the high mortality of females between 2.5 and 4.5 years of age and the resulting male-biased adult sex ratio. The majority of groups contained more than one probable male breeder. Polyandrous groups included both related and unrelated males. Behavioral differences between Cocha Cashu tamarins and other studied populations may result from the pressures of living in an environment inhabited by nine other primate species and numerous predators. © 1996 Wiley-Liss, Inc.     

Species and subspecies specificity in urine and scent marks of saddle-back tamarins (Saguinus fuscicollis)

Saguinus fuscicollisproduces scent marks which consist mainly of a mixture of urine and the secretions of circumgenital scent glands. The present study investigates the ability of saddle-back tamarins to discriminate between scent material from conspecifics and corresponding material from other species and to differentiate material from two subspecies of Saguinus fuscicollis.When choices between urine samples from conspecifics and from guinea pigs and choices between urine samples from conspecifics and from common marmosets were offered, the tamarins investigated samples from conspecifics more frequently. Similar responses were obtained when choices between scent marks from saddle-back tamarins and from common marmosets and between scent marks from saddle-back and red-chested moustached tamarins were offered. The tamarins also discriminated between scent marks and between extracts of scent marks from Saguinus f. fuscicollisand Saguinus f. illigeri.In these choice tests, subjects of both subspecies tended preferentially to investigate material from Saguinus f. fuscicollis.The results of these studies show that urine and scent marks contain chemical cues on which recognition of conspecifics can be based. Moreover, the scent marks of closely related subspecies also offer cues which could enable the tamarins to discriminate between them.     

A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis)

The author made an ecological study of the black-mantle tamarin (Saguinus nigricollis) in the primary forest in the basin of the River Caquetá in the upper Amazon in Colombia for 88 days during a study period from August 1975 to February 1976. The tamarin group repeats three activity patterns — feeding, resting, and moving — regularly in a day. In their feeding activity, the tamarins preferred to eat small insect and resin. They showed a special liking for large grasshoppers, 6–8 cm long, and spent much of the day to capture them. Moving in search of the grasshoppers, which are hard to capture in the forest, is closely related to the tamarin group's daily nomadism. From this evidence it can be concluded that the behavior which forms the basis of the tamarins' daily activity is the hunting of grasshoppers. In the transition time from the feeding activity, principally the hunting of grasshoppers, to the resting activity, a fruit eating behavior was always observed. At this time the tamarins ate well-ripened sweet fruit intensively for a short time. This behavior is thought to have the effect, in one respect, of easing strained relations arising among group members during the grasshopper hunting activity. It was also observed that mother tamarins shared their hard-to-capture grasshoppers with their offspring although the latter had already become independent of their mothers. In general, the tamarins lived in a small and compact group consisting of an adult male, an adult female, and their offspring. Some of these small groups had amicable interrelationships and often moved together, whereas other groups kept aloof from each other. These facts indicate that, besides the groups as the social units, large-groups comprising some of these unit groups moving together, exist in the social structure of the tamarins, and form the upper structure of the social unit. See the note added to the end of this article.