The impact of cropping on wild populations of Saguinus mystax and Saguinus fuscicollis in Peru

A transect census technique was used to estimate the population densities of Saguinus mystax and Saguinus fuscicollis at two sites in Peru. Cropping of these two species had occurred five years before the census at one site and two years before at the other. The populations of S. mystax at both sites had recovered completely from cropping, and the relationship between S. mystax and S. fuscicollis had not been altered at one site and had been reversed in favor of S. mystax at the other.     

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.     

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.     

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.     

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.     

Spontaneous colitis cystica profunda in captive tamarins

Of the 232 tamarins (133 Saguinus mystax and 99 Saguinus labiatus) that died at the Center for Reproduction and Conservation of Nonhuman Primates in Iquitos, Peru from January 1987 to December 1990, 23 monkeys (9.9%) were diagnosed as having chronic colitis. Typically, the cecal and colonic mucosa was greyish and small yellowish cysts, measuring 1–4 mm, were found randomly distributed bulging the mucosa. Microscopically, colitis cystica profunda was diagnosed additionally in six more animals, giving a total of 29 cases (12.5%). This is the first report to our knowledge that describes colitis cystica profunda in a nonhuman primate.     

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.     

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.     

Biochemical diversity and genetic distance in two species of the genusSaguinus

A comparative study of 20 blood genetic systems was performed on three populations of genusSaguinus: S. fuscicollis weddelli, S. midas niger, andS. midas midas. Some markers are useful for the characterization of the two species.ADA ⁵, ADA⁶, CA2³, CA2⁴, andES2 ² occur only inS. fuscicollis whileADA ⁴is fixed inS. midas. S. midas midas showed heterozygosity value comparable to those previously obtained for the genusAlouatta. Estimates of genetic distance betweenS. fuscicollis andS. midas species of about 14% are in accordance with those referred to in the literature for interspecific differences. Genetic distances between subspecies ofSaguinus midas were nearly 3%, which is within the range for subspecies.     

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.     

A comparative study of positional behavior in three species of tamarin monkeys

Tamarins of the genusSaguinus are small-bodied New World monkeys that exhibit clawlike or modified nails. Patterns of positional behavior and habitat utilization are presented for three species,Saguinus fuscicollis, S. geoffroy, andS. mystax. These data were collected on free-ranging tamarin populations in Panama and Peru. Despite considerable differences in body weight, all three species exhibited very similar patterns of positional behavior, with quadrupedal bounding and running accounting for 43 – 52% of travel time. Leaping was the second most common locomotor activity and accounted for 31 – 41% of travel. Although each species leaped principally on small supports in the perimeter of the tree crown, approximately 20% of all leaps inS. fuscicollis involved moderate to large sized vertical trunks located in the undercanopy. Leaping between trunks was rare in the two larger tamarin species. Measurements taken on live wild-trapped adults reveal that compared toSaguinus geoffroyi andS. mystax, S. fuscicollis is characterized by a long legspan and an especially long armspan. It is proposed that inS. fuscicollis, elongated forelimbs play an important role in maneuvering and rotating the body during the in-air phase of trunk-to-trunk leaping, and increase the breaking distance needed to decelerate the body upon impact. Additional relationships between body size, substrate preference, and positional behavior in callitrichines are discussed.     

Taxonomic status of Saguinus tripartitus (Milne-Edwards, 1878)

A review of specimens and field notes of Carlos Olalla and his sons showed that they collected Saguinus tripartitus and Saguinus fuscicollis lagonotus at the same place on the right bank of the lower Rio Napo in Peru. Thus, these two forms are sympatric, although they probably occur in different habitats. Therefore, Saguinus tripartitus should be treated as a distinct species, not as a subspecies of Saguinus fuscicollis.     

Primary renal hemangiosarcoma in a moustached tamarin

A wild-caught adult female Saguinus mystax died after 54 months in captivity. At necropsy, a small reddish zone in the renal cortex of one kidney was shown histologically to be a hemangiosarcoma.     

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.     

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.     

A New Subspecies of <Emphasis Type="Italic">Saguinus fuscicollis</Emphasis> (Primates,Callitrichidae)

Saddleback tamarins (Saguinus fuscicollis, S. melanoleucus, and S. tripartitus) occur in the upper Amazon, west of the rios Madeira and Mamoré–Guaporé to the Andes. They currently comprise 13 species and subspecies in Bolivia, Brazil, Colombia, Ecuador, and Peru. Here we report on a previously undescribed subspecies of Saguinus fuscicollis from the interfluvium of the lower rios Madeira and Purus in the central Amazon of Brazil. It is a distinct form with a very pronounced mottling on the back giving the appearance of a saddle, a characteristic shared by the 3 species, and the reason for their collective common name. The lack of a white superciliary chevron and its highly mottled ochraceous-dark brown to black saddle that extends from the scapular region to the base of the tail distinguish the new taxon from Saguinus fuscicollis weddelli. The latter characteristic also distinguishes it from another saddleback tamarin (Saguinus fuscicollis ssp.) that has been reported immediately to the south of its range in the same interfluvium. We compare pelage coloration, external characters and craniometric measurements with its geographically closest relatives, Saguinus fuscicollis weddelli and S. f. avilapiresi, and indicate its probable geographic distribution in a small area between the rios Madeira and Purus, just south of the Rio Amazonas.     

Polymorphic microsatellite loci for the mustached tamarin (Saguinus mystax) and their cross‐species amplification in other New World monkeys

We isolated and characterized 10 polymorphic microsatellite loci for the mustached and cotton‐top tamarin (Saguinus mystax and S. oedipus) and also tested their applicability in other New World monkey genera. Six loci proved to be variable in Cebus apella and Saimiri sciureus/S. boliviensis, respectively. We also show that faeces‐derived DNA is suitable for polymerase chain reaction (PCR) analyses of a primate taxon that gives birth to twins with individuals exhibiting a haematopoetic chimaerism. The microsatellite fingerprint patterns do not display a complex mixture of the PCR‐products derived from the alleles of both dizygotic twins, but exhibit the constitutive alleles of one sibling only.     

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.     

Effects of support size and orientation on symmetric gaits in free-ranging tamarins of Amazonian Peru: implications for the functional significance of primate gait sequence patterns

The adoption of a specific gait sequence pattern during symmetrical locomotion has been proposed to have been a key advantage for the exploitation of the fine branch niche in early primates. Diverse aspects of primate locomotion have been extensively studied in technically equipped laboratory settings, but evolutionary conclusions derived from these investigations have rarely been verified in wild primates. Bridging the gap from the lab to the field, we conducted an actual performance determination of symmetrical gaits in two free-ranging tamarin species (Saguinus mystax and Saguinus fuscicollis) of Amazonian Peru by analyzing high-speed video recordings of naturally occurring locomotor bouts. Tamarins arguably represent viable models for aspects of early primate locomotion. We tested three specific hypotheses derived from laboratory studies to test for the influence of support size and orientation and to gain further insight into the functional significance of primate gait sequence patterns: (1) The tamarins utilize symmetrical gaits at a higher rate on small supports than on larger ones. (2) During symmetrical locomotion on small supports, diagonal sequences are utilized at a higher rate than on larger supports. (3) On inclines, diagonal sequences are predominantly used and on declines, lateral sequences are predominantly used. Our results corroborated hypotheses 1 and 3. We found no clear support for hypothesis 2. In conclusion, our results add to the notion that primate gait plasticity, rather than uniform adoption of diagonal sequence gaits, enabled early primates to accommodate different support types and effectively exploit the small branch niche.     

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.