Tamarin polyspecific associations: Forest utilization and stability of mixed-species groups

Niche separation is likely to play a key role in the formation of mixed-species groups. Saddle-backed tamarins (Saguinus fuscicollis) were studied at three sites with different primate communities in northern Bolivia: (1) with red-bellied tamarins,S. labiatus; (2) with emperor tamarins,S. imperator; and (3) without a congeneric species. The degree of association is higher betweenS. labiatus andS. fuscicollis than betweenS. imperator andS. fuscicollis and is related to differences in forest utilization between associating pairs. Niche separation is found to be greater betweenS. labiatus andS. fuscicollis than betweenS. fuscicollis andS. imperator. The mean height and habitat utilization ofS. fuscicollis does not differ greatly across the three sites, nor does the height of tamarins in and out of association. It is concluded that combined with differences in body size and dietary overlap, vertical segregation plays an important role in tamarin polyspecific associations (increasing the potential of both foraging and anti-predatory benefits) and that this is not a consequence of vertical displacement ofS. fuscicollis by its dominant congeners.     

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.     

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.     

Ecological study of the saddle backed tamarin (Saguinus fuscicollis) in Northern Bolivia

The author carried out an ecological survey of the saddle backed tamarin (Saguinus fuscicollis) in the Pando, northern Bolivia, from July to December 1979. It was found thatS. fuscicollis formed a family group consisting of two to seven individuals and spent almost all the daytime in moving to forage insects, although it fed mainly on fruits of the family Moraceae. Primary forest was preferred for sleeping sites, whereas the animals spent more hours in secondary forest than in primary forest in their home range. Marking sites were concentrated in the center of the home range but encounter behaviors tended to take place near the borderlines of the home range. It was also found that infants began feeding on fruit at about 5 weeks of age, whereas they shared insects obtained by their mothers until about 10 weeks of age.     

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.     

Systematics of the Saguinus oedipus group of the bare-face tamarins: Evidence from facial morphology

The systematics of the Saguinus oedipus group within the bare-face tamarins remains open to question. Hershkovitz (Living New World Monkeys (Platyrrhini), Vol. 1. Chicago: University of Chicago Press, 1977) places the cotton-top and rufus-naped tamarins as subspecies of Saguinus oedipus (S. o. oedipus and S. o. geoffroyi, respectively). In contrast, several other authors have argued that these two taxa should be considered separate species (S. oedipus and S. geoffroyi). Phylogenetic relationships within the group are also disputed. Resolving these different interpretations has been difficult in part because no study of this group has included an objective measure of expected levels of specific vs. subspecific variation. We used facial measurements from 179 adult crania to address the systematics of this group and included a related species that is known to include multiple subspecies. Our sample included three taxa from the S. oedipus group of the bare-face tamarins (S. oedipus, S. geoffroyi, and S. leucopus) and six subspecies from the related hairy-face tamarin species S. fuscicollis. Comparisons to S. leucopus provided a relative measure of species-level differences. Analyses that included S. fuscicollis provided a measure of subspecific variation. There was no evidence of facial sexual dimorphism in any of these taxa. A variety of multivariate statistical analyses including discriminant function and cluster analysis suggest that S. oedipus and S. geoffroyi differ morphologically at a level consistent with species-level distinctions. The extent of differences between these taxa is large. The differences in their facial morphology was on the order of differences between S. oedipus or S. geoffroyi and S. leucopus rather than the extent of variation among S. fuscicollis subspecies. Furthermore, a comparison of collecting localities revealed that the variation we observed among S. oedipus and S. geoffroyi was not clinal but presented a large morphological discontinuity at the boundary between taxa. Our analyses also suggested that S. leucopus is more similar to S. oedipus than is either to S. geoffroyi. Finally, it may be that there are some distinct species within the S. fuscicollis group. However, this hypothesis, along with other phylogenetic relationships suggested by this study, will require more data and further study. © 1992 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.     

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.     

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.     

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.     

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.     

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.     

Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis

From field data collected in the Amazon Basin of northeastern Peru, I present evidence that moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarins maintain detailed knowledge of the distribution and location of many tree species in their home range. During the wet season months of October through December 1984, fruits and exudates from 20 tree species and over 150 individual trees accounted for 75% of plant feeding time. These trees exhibited a patchy distribution; mean nearest-neighbor distances between trees of the same species averaged 148 meters. Moustached and saddle-back tamarins visited an average of 13 trees per day, concentrating their feeding efforts on 4–11 individual trees from a small number of target species. In 70% of all cases the nearest tree of a given species was selected as the next feeding site. Movement between these sites was characterized by relatively straight-line travel. It is argued that S. mystax and S. fuscicollis offset the patchiness component of the fruit and exudate part of their diet through goal-directed foraging and an ability to compare accurately the distances and directions from their present location to a large number of potential feeding trees.     

The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis)

Data collected during a 12-month field investigation of mixed species troops of Saguinus mystax and Saguinus fuscicollis in the Amazon Basin of north-eastern Peru indicate that callitrichid primates play an important role in tropical forest seed dispersal. Moustached and saddle-back tamarins were observed to ingest seeds from a variety of tree and liana species and pass them unharmed. These seeds tended to be large and heavy, and passed through the tamarin digestive tract in one to three hours. Experimental plantings of defecated seeds yielded a germination success rate of 70%. The specific gravity of these seeds (weight/volume) was inversely correlated with passage time and apparently had an indirect influence on the distance that seeds were dispersed from the parent tree. In the case of three preferred fruiting species, Leonia glycycarpa, Pourouma sp., and Hippocrateaceae #283, the present distribution of adult trees closely resembled the pattern of the seed shadow created by Saguinus. Moustached and saddle-back tamarins appeared to be reliable and high-quality dispersal agents for a number of tree and liana species. In this role, they are likely to exert an important influence on the composition, distribution, and regeneration patterns of Amazonian rain forest.     

Effect of Resting Patterns of Tamarins (<Emphasis Type="BoldItalic">Saguinus fuscicollis</Emphasis> and <Emphasis Type="BoldItalic">Saguinus mystax</Emphasis>) on the Spatial Distribution of Seeds and Seedling Recruitment

The spatial distributions of dispersed seeds have important evolutionary consequences for plants. Repeated defecations in sites frequently used by seed dispersers can result in high seed concentrations. We observed the resting behavior of a mixed-species group of tamarins in Peru and recorded the occurrence of seed dispersal (over 8 mo) and seed fate (over 11–22 mo) to determine whether the location and use of resting sites influenced the spatial distribution of dispersed seeds and seedlings. The tamarins rested mostly on trees (Saguinus fuscicollis: 60.6%, S. mystax: 89.2%) and dead trunks (S. fuscicollis: 24.4%) and used 61% of their resting sites repeatedly. During both the dry and wet seasons, tamarins dispersed significantly more seeds within resting areas (0.00662 and 0.00424 seeds/m², respectively) than outside them (0.00141 and 0.00181 seeds/m²). Seed survival and seedling recruitment did not differ significantly between resting and other areas, resulting in a higher seedling concentration around the resting sites. Seed density did not increase with the duration or the frequency of use of the resting sites but did increase when we pooled the seasonal resting sites together in 50 m × 50 m quadrats, ultimately causing a clumped distribution of dispersed seeds. The use of resting sites in secondary forest, particularly during the dry season, allows the creation of seedling recruitment centers for species coming from the primary forest. Our findings show that tamarin resting behavior affects the spatial distribution of dispersed seeds and seedlings, and their resting sites play an important role in plant diversity maintenance and facilitate forest regeneration in degraded areas.     

Dietary Differences Among Sympatric Callitrichinae in Northern Bolivia: Callimico goeldii,Saguinus fuscicollis and S. labiatus

Studies of sympatric species can provide important data to define how dietary and habitat requirements differ among them. I collected dietary data during a first yearlong comparative study of wild groups of Callimico goeldii, Saguinus labiatus and S. fuscicollis. Dietary overlap was highest between Saguinus fuscicollis and Saguinus labiatus throughout the year, and lowest between Saguinus labiatus and Callimico goeldii. All three species had high dietary overlap in February and March when a few abundant fruit species dominated their diets. Although all three species rely heavily on many of the same fruits and arthropods, there are several important distinctions among their diets. Surprisingly, Callimico goeldii consume large quantities of fungus throughout the year: 29% of annual feeding records. Mycophagy is more frequent in the dry season when fruits are scarce. In contrast, Saguinus labiatus rarely eat fungus during the period of fruit scarcity, and instead rely on nectar, a resource never exploited by Callimico goeldii. Saguinus fuscicollis also rely on nectar during periods of low fruit availability and increase their intake of arthropods and exudates. During April, a period of fruit scarcity, exudates comprise >50% of the feeding records of Saguinus fuscicollis. The use of different food resources during fruit scarcity, and differences in the heights at which each species feeds and forages appear to define a distinct ecological niche for each of them and allow them to maintain long-term associations throughout the year. Furthermore, I hypothesize that the limited distribution of Callimico goeldii may result from their restriction to forests that have high disturbance rates, where microhabitats appropriate for fungal growth are abundant, but which also contain abundant fruit and insects.     

Gut morphology of Callithrix nigriceps and Saguinus labiatus from western Brazilian Amazonia

Quantitative data on the gut proportions of the recently-described black-headed marmoset (Callithrix nigriceps) from western Brazilian Amazonian are presented. Like other marmosets, C. nigriceps exhibits a relatively large caecum and colon associated with adaptations for gummivory. The degree of gut specialisation recorded is greater than that for any other platyrrhine for which quantitative data are available. Gum was found in the stomach contents of all four individuals examined, although the fruit/seeds of as many as seven different plant taxa were also encountered, in addition to insects of six different orders. Gut proportions of two Saguinus labiatus from the same region were typical of the more frugivorous tamarins, and stomach contents included only fruit and insects. Relative gut proportions of both species were closely similar to those of congeners from the same region. © 1993 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.     

Historical biogeography of tamarins,genus Saguinus: the molecular phylogenetic evidence

Hypotheses of the historical biogeography of tamarins (genus Saguinus) based on variation in coat colors and body size are tested using phylogenetic relationships inferred from mitochondrial DNA (mtDNA) sequence data. Samples from all 12 species of Saguinus and several subspecies are included in the analysis. Approximately 1,200 bases of mtDNA sequence from the cytochrome b and D-loop regions are reported for the tamarins and several outgroup taxa. Parsimony analysis of the mtDNA sequence data reveals Saguinus to be a monophyletic taxon composed of two major clades: one, the Small-bodied clade, contains S. nigricollis, S. tripartitus, and S. fuscicollis, and the other, the Large-bodied clade, contains the other nine species. The phylogenetic relationships among tamarins inferred from the mtDNA sequence data reject previous hypotheses for the historical biogeography of tamarins and suggest different dispersal routes for this group of New World monkeys. The molecular data suggest that tamarins dispersed across South America in two major waves from an origin somewhere south of the Amazon. One wave moved in a westerly direction, whereas the other moved in a northeastern direction toward the Amazon delta and then west along the northern portion of the continent into northern Colombia and Panama. Am J Phys Anthropol 108:65–89, 1999. © 1999 Wiley-Liss, Inc.     

Habitat Use and Ranging Behavior of <Emphasis Type="Italic">Callimico goeldii</Emphasis>

We studied the diet, habitat use, and ranging behavior of 1 group of Callimico goeldii (callimicos) over 12 mo in northwestern Bolivia. The group’s diet was comprised of fungi (39%), fruits (31%), arthropods (14%), exudates (14%), and other matter (2%). Callimicos concentrated their ranging activities in secondary forest (50%), primary forest with dense understory (30%), and bamboo (17%) habitats. The group’s total home range was 114 ha; on average they used 38.4 ha/ mo and had a day range of 925 m. Monthly average day ranges—but not monthly home ranges—increased as frugivory declined, suggesting that subjects foraged on fungi and exudates by rechecking resources within a core area, making their day ranges longer than during months when they concentrated on fruit resources. The callimicos formed polyspecific associations with tamarins (Saguinus labiatus and S. fuscicollis) during 81% of observations. Day ranges increased in months with higher association rates which appears to result from the callimicos using a broader set of habitats when with tamarins than when alone. The ranging pattern of callimicos appears to be influenced primarily by 3 factors: their seasonal shift in diet requires that they forage in a variety of habitats across the year; their depletion of resources causes them to shift their core area over time; and their lack of territorial behavior eliminates the need to patrol boundaries as part of their daily movement. As a result, callimicos differ from many other callitrichids in their low ratio of day range length to home range size.