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.     

Leaders of progressions in wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax), with emphasis on color vision and sex

Leadership of travel progression is an important aspect of group living. It is widely believed that trichromacy evolved to facilitate the detection and selection of fruit in the dappled light of a forest. Further, it has been proposed that in New World primate species, which typically contain a range of color vision phenotypes, at least one female in a group will be trichromatic (i.e., having three types of visual pigment, in contrast to the two types of pigment found in dichromatic individuals) and will lead the group to fruiting trees. We examine progression leadership within two wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins over a complete year. As whole units, the mixed-species troops were most frequently led by a mustached tamarin. This is the first time that mixed-species group leadership and individual leadership have been quantified in these tamarin species. In terms of single-species intragroup leadership, neither the visual status (dichromatic or trichromatic) nor the sex of individuals had a consistent effect across species. Saddleback tamarin groups were led by males more frequently than females, while evidence suggests that mustached tamarins may be female-led. The notion that all groups contain at least one trichromatic female that leads the troop to feeding trees was not supported.     

Functions of Intermittent Locomotion in Mustached Tamarins (<Emphasis Type="Italic">Saguinus mystax</Emphasis>)

Many animals interrupt their moving with brief pauses, which appear to serve several different functions. We examined the function of such intermittent locomotion in wild living mustached tamarins (Saguinus mystax), small arboreal New World primates that form mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We investigated how different environmental and social factors affect pausing during locomotion and used these data to infer the function of this behavior. As measures of intermittent locomotion, we used percentage of time spent pausing and pause rate. We considered 3 possible functions that are not mutually exclusive: increased endurance, route planning, and antipredator vigilance. Mustached tamarins spent on average (mean ± SE) 55.1 ± 1.0% of time pausing, which makes effective resource exploitation more time consuming and needs to be outweighed by correspondingly large benefits. Percentage of time spent pausing decreased in larger mixed-species groups vs. smaller mixed-species groups and decreased with height and in monkeys carrying infants. It was not affected by sex, age, spatial arrangement, or single-species group size. Pause rate increased in individuals traveling independently compared to those traveling in file, but was not affected by other factors. The group size effect in mixed-species groups lends support to the notion that pausing during locomotion is an antipredator tactic that can be reduced in the increased safety of larger groups, but other results suggest that additional functions, particularly route planning, are also of great importance. Benefits in terms of predator confusion and group movement coordination are also likely to play a role and remain a topic for further research.     

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.     

Responses of Captive Single- and Mixed-Species Groups of Saguinus to Novel Nonthreatening Objects

The provision of novel objects allows one to probe for behavioural differences among species. This is particularly relevant when studying species that form mixed-species groups, as divergent responses may provide clues to the advantages that individuals gain from associating. We compared the responsiveness to novel objects in captive single- and mixed-species groups of saddleback (Saguinus fuscicollis) and red-bellied (Saguinus labiatus) tamarins to determine the influence of a congener. We tested groups with novel objects placed near the top, the middle, and on the floor of their enclosures and measured latency to approach and touch them. We tested predictions related to differences in lifestyle patterns under natural conditions. As we predicted, S.labiatus, which usually occur at a higher mean height in the forest than their congeners, responded to objects placed near the top of the enclosure significantly quicker in both single- and mixed-species groups. S. fuscicollis responded to objects placed on the floor quicker, and in mixed-species groups S. fuscicollis approached them before S. labiatus did. There were specific differences in median touch–approach time (T-A): Saguinus fuscicollis had a shorter T-A time than that of S. labiatus, which can be related to their manipulative foraging style. Reaction times decreased in mixed-species trials for both species, suggesting that the reaction of one species may effect the congener. Both species may benefit through association, though the dominance of Saguinus labiatus over S. fuscicollis may limit the advantages to S. fuscicollis. Over all our study supports the idea that cross-specific social facilitation is an important consequence of mixed-species groups of Saguinus.     

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.     

The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (<Emphasis Type="Italic">Saguinus fuscicollis</Emphasis>)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.     

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.     

Interindividual distances in mixed-species groups of ants: an estimation of cohesion in social groups

Spatial organization was estimated in mixed-species groups of ants with interindividual distance measures as a function of: (1) the age of the workers when associated; and (2) the presence of the brood. Workers ofManica rubida (Myrmicinae) andFormica selysi (Formicinae) were reared in single-species groups (control) or in artificial, mixed-species groups, created 5 h, 12 h or 22 h after emergence, with or without brood. By recording the location of each individual in the nest during the 10 days following the creation of the groups, we evaluated the spatial organization and the interindividual distances between homocolonial or allospecific workers, and between workers and homocolonial or allospecific brood. The cohesion of the group, depend on the age of the workers when associated: the younger the individuals are when the groups are created, the smaller are the interindividual distances. Moreover, homocolonial individuals aggregated with brood, when present, which improves the overall cohesion of the group. However, in mixed groups, both species associated preferentially with members of their own species. This suggests that newly-emerged ants do not depend totally on the odors of their nestmates to construct their recognition template and that they also possess an innate, specific template.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Food patch structure and plant resource partitioning in interspecific associations of amazonian tamarins

ávila-Pires’ saddle-back tamarins (Saguinus fuscicollis avilapiresi) and red-cap moustached tamarins (S. mystax pileatus), coexisting in highly stable mixed-species groups, overlapped considerably in their use of plant food resources at an Amazonian terra firme forest site. Overlap between food types consumed by the two species was particularly high during periods of lowest fruit availability, when they resorted to a common food supply, primarily the pod exudates of two emergent species of legume trees (Parkia nitida andParkia pendula) and nectar ofSymphonia globulifera. Within-group interspecific competition did not covary with independent measures of resource availability, contrary to predictions based on resource partitioning models. A greater number of both saddle-back and moustached tamarins were able to feed for longer patch residence periods within larger and more productive food patches, whereas small and clumped patches could be monopolized by the socially and numerically dominant moustached tamarins to the physical exclusion of the smaller-bodied saddle-back tamarins. Overall rates of interspecific aggression were extremely low, however, partly because patches that could be monopolized contributed with a minor proportion of either species’ diet. Saddle-backs foraged at lower levels in the understory and encountered smaller food patches more often, whereas moustached tamarins foraged higher and encountered more larger patches in the middle canopy. Although the two species led one another to differently-sized patches, moustached tamarins initiated most feeding bouts and encountered significantly larger and more productive patches that tended to accommodate the entire mixed-species group. Disadvantages of exploitative and interference feeding competition over plant resources, and advantages of shared knowledge of food patches, are but one component of the overall cost-benefit relationship of interspecific associations in tamarins.     

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.     

Active formation of mixed-species grouse leks: a role for predation in lek evolution?

Behavioural ecologists have interpreted avian leks as products of sexual selection, in which males display socially to increase their opportunities to mate. However, without invoking reproductive queuing or kin selection, this paradigm does not necessarily explain why many males that fail to mate participate in leks. An alternative solution, that males also aggregate to reduce predation, has previously lacked compelling support. We show that mixed-species leks, comprising two congeneric grouse, form when single males or small groups of one species, the greater prairie chicken Tympanuchus cupido, join leks of another, the sharp-tailed grouse T. phasianellus. We documented the process by observing lek dynamics and comparing group sizes between mixed- and single-species leks. Joining implies that prairie chickens benefit from displaying with sharp-tailed grouse. The numbers of females of each species attending a lek increased with the number of conspecific, but not heterospecific, males. This suggests that the joining of heterospecifics is unlikely to increase mating opportunities, and leaves lowered predation risk as the most likely benefit of associating with heterospecifics. Active formation of mixed-species leks therefore suggests that predation may be sufficient to drive lek formation. The benefits of participation in mixed leks may be asymmetrical because prairie chickens display more and are less vigilant than sharp-tailed grouse.     

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.     

Family Feuds: Severe Aggression among Cooperatively Breeding Cotton-Top Tamarins

A survey of severe aggression occurring over the 20 year history of a cotton-top tamarin (Saguinus oedipus) colony indicated that most aggression was between same-sex individuals, with fights among siblings more common than parent-offspring conflict. Males engaged in severe aggression more often than females did, paralleling the dimorphic aggressive response to same-sex intruders in this species. Female-female aggression occurred at larger group sizes than male-male aggression, suggesting a higher threshold for female aggression. Much sibling aggression was directed by postpubertal subadults toward prepubertal siblings. Only 17% of aggression occurred in association with infant births, and these cases rarely involved parents and offspring suggesting that aggression was not used by reproductive animals to defend their breeding position. Severe aggression was often associated with attempts to introduce stepparents or movement of individuals in and out of the group. The mean group sizes when aggression is observed in captivity are close to the maximum group sizes observed in wild tamarins, which suggests that severe aggression in captive groups may reflect processes related to dispersal in wild tamarins.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

Antiphonal Responses to Loud Contact Calls Produced by Saguinus oedipus

We report the results of an experiment designed to investigate whether captive cotton-top tamarins (Saguinus oedipus) selectively call back to an absent cagemate. We removed 2 individuals living in separate cages (cycling through the colony so that each individual was removed 10 times) from the homeroom and played back calls produced by one of them. The caller's cagemate, residing in the homeroom, was more likely to be the first individual to call back antiphonally than any other individual in the colony was. In support of previous work using both habituation-discrimination and phonotaxic techniques, our results show that cotton-top tamarins can recognize cagemates and possibly individuals by voice alone, and that the antiphonal playback method provides yet another tool for investigating acoustic perception in nonhuman primates.     

On the Advantages of Mixed‐Species Groups: Impalas Adjust Their Vigilance When Associated With Larger Prey Herbivores

Prey can obtain valuable benefits from associating with other species if heterospecifics help to detect predators or locate good food patches. In mixed‐species groups, how species respond to the presence of other species remains a poorly explored question although it might give crucial insights into mechanisms underlying the interspecific coexistence. We studied temporary mixed‐species groups of large herbivores in Hwange National Park (Zimbabwe) between the common impala (Aepyceros melampus), the focal species here, and bigger species including the plains zebra (Equus quagga), the greater kudu (Tragelaphus strepsiceros) or the blue wildebeest (Connochaetes taurinus). In the Hwange savanna, the focal and smaller species are exposed to a larger range of predators than the associated species. In this context, we investigated how impalas adjusted their vigilance with group size comparing impala‐only and mixed‐species groups and whether the identity of heterospecifics affected vigilance of impalas. Our study showed that the time impalas spent in vigilance significantly decreased with group size when they formed impala‐only groups, whereas it did not significantly vary with group size in mixed‐species groups. Moreover, in mixed‐species groups, impalas did not adjust their time spent in vigilance with the proportion of conspecifics and the identity of the associated species. Thus, the mechanism underlying the difference of impalas' behavioural adjustment of vigilance with group size between single‐ and mixed‐species groups seemed to be related to the presence but not to the number and the identity of heteropecifics. Finally, we discuss the concept that larger and dominant heterospecifics were likely to increase competition for food access, thereby forcing higher vigilance of impalas, outweighing any reduction from collective vigilance.     

Vigilance responding to number of conspecifics among mixed groups of cranes in demilitarized zone

Numerous studies have addressed antipredatory benefits of mixed-species flocks of foragers, but studies on individual's vigilance as a function of group size are limited. In the Cheolwon area of the Korean Demilitarized Zone, vigilance of the subordinate White-naped cranes (Grus vipio) in 11 groups composed of conspecifics and the dominant Red-crowned cranes (Grus japonensis) was examined. Vigilance correlated negatively with group size due to negative correlation with the number of conspecifics, but not the dominant heterospecifics. This is consistent with the hypothesis that a decrease in vigilance in larger groups is due to antipredatory benefits from increased predator detection in larger groups (associated with the presence of a larger number of conspecifics). This suggested that the mechanism leads to canceling out of the otherwise expected antipredatory benefits to the subordinate species from the increased predator detection by larger group size (associated with larger number of dominants). This is one of only a few behavioral studies of these endangered crane species in the relatively inaccessible wintering area of international importance in the areas of high conservation value.     

A field study on the red-bellied tamarin,Saguinus l. labiatus,in Bolivia

A 5-month field study was conducted on red-bellied tamarins,Saguinus labiatus labiatus, in the Pando Department of northern Bolivia. Group sizes ranged from 5 to 10 animals, and each group associated with a group of saddle-backed tamarins,Saguinus fuscicollis weddelli. Members of three groups were trapped and marked and data were collected by radiolocation. The average range size used over 10 days was 19 ha. On average the groups entered about 29% of their range each day and had a mean daily path length of about 1487 m. The groups used a number of different sleeping sites within their ranges. They fed on a variety of different fruits and also on nectar from flowers, resin, and insects. Areas within the home range which were used significantly more than expected were generally those in which one or more of the following existed: a sleeping site, an intergroup encounter site, or a site where the group took shelter during an extended period of heavy rain.