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.     

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.     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.     

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.     

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.     

Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest

The feeding ecology of two small-bodied primate species—saddle-back ( Saguinus fuscicollis auilapiresi ) and moustached tamarins ( S. mystax pileatus )—occurring in stable, mixed-species groups was studied in a terra firme forest site in the upper Urucu River, Amazonas, Brazil. Ecological data are based primarily on one mixed-species group of 5–8 saddle-back and 8–10 moustached tamarins. The overall vegetative and animal-prey components of each tamarin species' diet, their selection of food species, and the seasonal variation in their use of plant resources are described, and compared to those of callitrichids elsewhere. The extremely diverse diet of tamarins included at least 136 tree, 33 vine and liana, 12 epiphyte and nine shrub species, as well as a wide range of prey items. They fed primarily on ripe fruit pulp of most of these species for most of the year, but shifted to floral nectar and plant exudates of a few key plant species during the dry season. Taxonomic overlap in plant diet was nearly complete between the two tamarin species, but they diverged considerably in their prey capture techniques. Saddle-backs used the low forest understorey, and manipulatively searched for sedentary prey concealed within discrete, usually rigid, microhabitats, whereas moustached tamarins used the midstorey where they visually searched for mobile prey well exposed on foliage. These and other feeding and foraging patterns are discussed in the light of other callitrichid species studied to date.     

Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis

Vertebrate predation was examined in sympatric moustached tamarins (Saguinus mystax) and saddle-back tamarins (Saguinus fuscicollis) in the Amazon rainforest of northeastern Peru. Both species prey on frogs and lizards, and very rarely on nestling birds. As a result of divergent foraging strategies, S. mystax primarily exploited frogs at higher strata of the forest, while S. fuscicollis predominantly preyed on reptiles in the lower strata and on the ground. This difference may strengthen the niche differentiation between these two tamarin species that exists with regard to other prey.     

Seed Swallowing in Tamarins: Evidence of a Curative Function or Enhanced Foraging Efficiency?

Nonhuman primates represent a major component of the frugivore biomass in several rain-forest communities. Although there is considerable evidence that prosimians, monkeys, and apes serve as dispersal agents for many tropical trees, little attention has been paid to the more basic questions of why certain species of primates swallow and void seeds, and what, if any, are the advantages to an animal of having a large, hard, bolus pass through its digestive tract. We examine patterns of fruit-eating and seed-swallowing in two species of free-ranging tamarins: Saguinus mystax and Saguinus geoffroyi. Fruits commonly eaten by tamarins contain large seeds surrounded by a fibrous and adhesive pulp or arilate seed coat. They generally swallow seeds and pulp together. Intact seeds are voided over a 1- to 3-h period. Measurements of 132 seeds naturally voided by Panamanian tamarins average 11.2 mm in length and 0.3 g. The greatest number of large seeds contained in the digestive tract of a single animal at one time was 13. In the case of moustached tamarins, we collected 220 seeds. Average seed length is 11.9 mm and average seed weight is 0.3 g. At the time of capture, one animal had 26 seeds in its digestive tract. In both tamarin species, there is evidence of sex-based differences in feeding behavior. Adult female moustached and Panamanian tamarins swallowed and voided seeds of larger size than adult males did. Seed size is positively correlated with pulp weight (p <. 001), therefore females were selecting food items with higher nutritional rewards than adult males did. Given their small body size and relatively short digestive tract, why do tamarins swallow such large seeds? Although several explanations are possible, we propose that the large number and size of undigested seeds continuously passing through the tamarin gut serve a curative role in mechanically dislodging and expelling intestinal parasites—Ancanthocephala (spiny-headed worms)—from their digestive tracts.     

Effects of Passage Through Tamarin Guts on the Germination Potential of Dispersed Seeds

Passage through tamarin guts may have an effect on seed germination potential. To examine these effects, and the variation between 2 sympatric tamarin species, we studied Saguinus mystax and S. fuscicollis in northeastern Peruvian Amazonia. For most of 39 plant species, neither germination success nor latency was modified by gut passage. Neutral effects on seed germination potential suggest that tamarins may fulfill criteria for effective seed dispersal.     

Body weights in mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons in Amazonian Peru

An investigation of body weights of members of mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons was conducted at the Rio Blanco Research Station in northeastern Peru. A total of 107 adult and subadult tamarin monkeys were trapped, measured, and released. Data collected indicate that mean body weights for adult male and female moustached tamarins are 564 gm and 626 gm, respectively, whereas for adult saddle-back tamarins these values are 412 gm and 411 gm. Subadults weighed 11-27% less than adults. Body weights recorded in this study are significantly greater than those previously reported for tamarins of the same species and age living in other areas of Amazonian Peru. We hypothesize that, in the case of moustached and saddle-back tamarins, advantages associated with feeding and foraging in mixed species troops facilitate greater efficiency in resource monitoring and result in the maintenance of larger body weights.     

Tamarins and Dung Beetles: An Efficient Diplochorous Dispersal System in the Peruvian Amazonia

Dung beetles fulfill several key functions in ecosystems but their role as secondary seed dispersers is probably one of the most complex ones. Various factors, such as seed characteristics, dispersal pattern induced by the primary disperser, season, and habitat, can affect the seed–beetle interaction. Particularly little is known about the fate of seeds primarily dispersed in small feces. The aim of this study was to investigate the effects of these factors on the dung beetle community (species composition, number and size of individuals) and its consequences on burial occurrence and depth of seeds primarily dispersed by two tamarin species. We captured dung beetles in a Peruvian rain forest with 299 dung‐baited pitfall traps to characterize the dung beetle community. Seed burial occurrence and depth were assessed by marking in situ 551 dispersed seeds in feces placed in cages. Among these seeds, 22.5 percent were buried by dung beetles after 2 d. We observed a significant effect of the amount of dung, season, time of deposition, and habitat on the number of individuals and species of dung beetles, as well as on seed burial occurrence and depth, while the tamarin species significantly influenced only the number and the size of dung beetles. This seed dispersal loop is particularly important for forest regeneration: small to large seeds dispersed by tamarins in secondary forest can be buried by dung beetles. These seeds can thus benefit from a better protection against predation and a more suitable microenvironment for germination, potentially enhancing seedling recruitment.     

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.     

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.     

Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability versus variability

From June through December, data were collected on the diet and ranging patterns of moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarin monkeys in the Amazon Basin of northeastern Peru. During this 7-month period, insects and nonleguminous fruits accounted for 83% of tamarin feeding and foraging time. Despite marked seasonal variation in rainfall and forest productivity, patterns of habitat utilization, day range, dietary diversity, resource exploitation, and activity budget remained relatively stable throughout the year. Moustached and saddle-back tamarins appear to solve problems of food acquisition and exploit patchily distributed feeding sites using a relatively limited set of foraging patterns. In general, these primates concentrate their daily feeding efforts on several trees from a small number of target plant species. These feeding sites are uncommon, produce only a small amount of ripe fruit each day, and are characterized by a high degree of intraspecific fruiting and flowering synchrony. Trees of the same species are frequently visited in succession, and individual feeding sites are revisited several times over the course of 1–2 weeks. This type of foraging pattern occurred during both dry and wet seasons and when exploiting fruit, nectar, legume, and exudate resources. Seasonal variation in the percentage of feeding and foraging time devoted to insectivory was also limited. In this investigation, there was no consistent evidence that temporal changes in overall forest fruit production had a major impact on the feeding, foraging, or ranging behavior of either tamarin species.     

Predation on Orthoptera and other orders in insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru

Kaytydids and related insects are an important component in the diets of moustached ( Saguinus mystax mystax ) and saddle-back tamarins ( Saguinus fuscicollis nigrifrons ). Based on preliminary data of captured prey, trends suggest that partitioning occurs regarding orthopterans as a limited food resource. Of species caputre as prey, only three were shared by both tamarin species. Saddle-back tamarins appeared to specialize more on understorey species (0-4 m), concentrating on pseudophylline katydids. Moustached tamarins incorporated a greater percentage of phaneropterine katydids from the lower to middle canopy into their diet of insects. Although most prey species were exposed to view during the diurnal feeding period of the tamarins, only the saddle-back tamarin fed on katydids that spend the day concealed from view within dead curled leaves. Differentiation of the prey spectrum may represent a critical pattern of niche differentiation in these two sympatric tamarin species, which show a high overlap in their plant food resources.     

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.     

Impact of the spatial uncertainty of seed dispersal on tree colonization dynamics in a temperate forest

An aggregated distribution of dispersed seeds may influence the colonization process in tree communities via inflated spatial uncertainty. To evaluate this possibility, we studied 10 tree species in a temperate forest: one primarily barochorous, six anemochorous and two endozoochorous species. A statistical model was developed by combining an empirical seed dispersal kernel with a gamma distribution of seedfall density, with parameters that vary with distance. In the probability density, the fitted models showed that seeds of Fagaceae (primarily barochorous) and Betulaceae (anemochorous) were disseminated locally (i.e. within 60 m of a mother tree), whereas seeds of Acer (anemochorous) and endozoochorous species were transported farther. Greater fecundity compensated for the lower probability of seed dispersal over long distances for some species. Spatial uncertainty in seedfall density was much greater within 60 m of a mother tree than farther away, irrespective of dispersal mode, suggesting that seed dispersal is particularly aggregated in the vicinity of mother trees. Simulation results suggested that such seed dispersal patterns could lead to sites in the vicinity of a tree being occupied by other species that disperse seeds from far away. We speculate that this process could promote coexistence by making the colonization rates of the species more similar on average and equalizing species fitness in this temperate forest community.     

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.     

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.     

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.