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.     

Prey foraging of red titi monkeys, Callicebus cupreus, in comparison to sympatric tamarins, Saguinus mystax and Saguinus fuscicollis

We compared the prey capture strategies of red titi monkeys, Callicebus cupreus, with those of sympatric mustached, Saguinus mystax, and saddleback tamarins, Saguinus fuscicollis, to examine whether animal prey is important in niche differentiation between these Neotropical primates. We collected data on strata and substrate use during foraging, on prey searching and capturing, and on prey type of two C. cupreus groups and one group each of S. mystax and S. fuscicollis during a 5-month field study in northeastern Peruvian Amazonia. Our results showed that C. cupreus differed both from S. mystax and S. fuscicollis in prey capture strategies: (1) C. cupreus used lower forest strata for prey search and capture than S. mystax and higher forest strata than S. fuscicollis. (2) C. cupreus captured prey on a higher variety of substrates than S. mystax and more often on open microhabitats compared to S. fuscicollis. (3) C. cupreus captured prey more often directly than S. mystax and rarely by manual search, in contrast to S. fuscicollis. (4) C. cupreus fed exclusively on arthropods and focused on Hymenoptera, in contrast to both tamarin species that focused on Orthoptera and included vertebrates in their diet. These findings indicate that animal prey plays a role in niche differentiation between C. cupreus and S. fuscicollis/S. mystax and might facilitate the coexistence of these three sympatric species.     

Interspecific variation of scent-marking behaviour in wild tamarins, Saguinus mystax and Saguinus fuscicollis.

The scent-marking behaviour of sympatric moustached, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis, was compared in order to explore interspecific differences and potential sources of variation. The author examined basic patterns of scent marking (types, intensity, complexity), substrate use (type, orientation, height), and social patterning of scent marking in three groups of S. mystax and one group of S. fuscicollis at the Estación Biológica Quebrada Blanco, Peruvian Amazonia. S. mystax and S. fuscicollis differed significantly in the relative frequency of different types, and in the intensity and complexity of scent marking. Only S. fuscicollis showed allomarking. They also differed significantly in the type, orientation and height of substrates used for scent marking which corresponded to general differences in substrate use. In S. fuscicollis, but very rarely in S. mystax, two or more group members marked the same site sequentially or simultaneously. 'Collective scent marking', i.e. simultaneous scent marking by most or all group members, occurred only in S. fuscicollis. Since both tamarin species live sympatrically in mixed-species groups, ecological factors are unlikely to account for the differences found in scent-marking behaviour (except for differences in substrate use). They probably relate to as yet unknown differences in social and reproductive strategies of the two 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.     

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.     

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.     

Variations in dental measurements between Saguinus species and their systematic relationships.

Multivariate analysis is applied to dental measurements of Saguinus species to analyse their systematic relationships. The shape distance between Saguinus midas midas and S. midas niger is larger than that between S. nigricollis and S. fuscicollis, both of which are generally recognized as valid species. In dental form, S. bicolor is the closest relative of S. midas. S. inustus is not linked to S. leucopus. S. geoffroyi and S. leucopus, as S. inustus shows closer affinity with S. labiatus and S. mystax than with the former 3 species.     

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.     

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.     

Hand specialization, sympatry, and mixed-species associations in callitrichines

Hand morphology in callitrichines (i.e., tamarins, marmosets, and Goeldi's monkey) is correlated with positional and foraging behaviors. This study examines hand shape in callitrichines using an allometric approach. It addresses a series of questions relating hand anatomy, insect foraging behavior, and resource partitioning in callitrichines. The main questions are: 1. Do the hands of Leontopithecus differ in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands of Saguinus fuscicollis adapted to manipulative foraging, and are they functionally similar to Leontopithecus' hands? 3. Is hand morphology in S. fuscicollis more similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollis and S. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, and S. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, and Callimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands of Leontopithecus are adapted for manipulative foraging and are relatively longer and more slender than the hands of other callitrichines. A similar pattern is observed in the hands of S. fuscicollis, S. tripartitus and S. nigricollis. These latter species, however, differ significantly in shape from all other tamarin species. Large differences in hand morphology are observed among tamarin species that form mixed-species troops. These anatomical differences may permit resource partitioning and coexistence among these closely related taxa. Hand shape, expressed as log HLGM (logged hand length divided by the geometric mean of all measurements), is a good predictor of manipulative and non-manipulative prey foraging techniques employed by callitrichines.     

Survey of Saguinus mortality in a zoo colony.

Six years of necropsy records from a zoo colony of four tamarin species (Saguinus oedipus, S. geoffroyi, S. imperator, and S. mystax) were examined. Mean age at death was 4.0 years, average length in the colony at time of death was 3.4 years. Annual mortality rate varied between 9 and 30%. Gross necropsy findings, histopathologic, and bacteriological results indicate primary cause of death as follows: peritonitis (26%), septicemia (14%), nephritis (5%), hepatitis (5%), pneumonia (2%), and others.     

Field observations of the golden-mantled tamarin, Saguinus tripartitus, on the Río Curaray, Peruvian Amazonia

During a primatological survey on the Río Curaray in north-eastern Peruvian Amazonia, observations on the ecology and behaviour of the golden-mantled tamarin, Saguinus tripartitus, were made. Two groups consisting of 6 and 9 individuals were observed. The diet of one group that was observed in some detail consisted of fruit, insects (tettigoniid orthopterans) and gums. Patterns of height use were very similar to those observed in saddle-back tamarins, Saguinus fuscicollis. This similarity and the lack of evidence for sympatry with either S. fuscicollis or S. nigricollis lead to the suggestion that S. tripartitus should be reconsidered as a subspecies of S. fuscicollis rather than a species on its own; alternatively, other subspecies of S. fuscicollis should be raised in taxonomic rank.     

Flower and Fruit Visitors of Marcgravia longifolia in Amazonian Peru

Abstract: We recorded nectarivorous and frugivorous visitors of Marcgravia longifolia (Marcgraviaceae) at the Estación Biológica Quebrada Blanco in the northeastern Peruvian Amazonia. M. longifolia belongs to the subgenus Plagiothalamium, with downward facing flowers. A glossophagine bat, probably Anoura caudifer, was identified as a potential pollinator. Three primate species - Saguinus fuscicollis, Saguinus mystax and Callicebus cupreus - were recorded as potential seed dispersers. This is the first documentation of primate seed dispersal of a species from the family Marcgraviaceae.     

The range of the golden-mantle tamarin, <Emphasis Type="Italic">Saguinus tripartitus</Emphasis> (Milne Edwards, 1878): distributions and sympatry of four tamarin species in Colombia,Ecuador, and northern Peru

A detailed understanding of the range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878), in Amazonian Peru and Ecuador is of particular relevance, not only because it is poorly known but also because it was on the basis of its supposed sympatry with the saddleback tamarin (S. fuscicollis lagonotus) that Thorington (Am J Primatol 15:367-371, 1988) argued that it is a distinct species rather than a saddleback tamarin subspecies, as was believed by Hershkovitz (Living new world monkeys, vol I. The University of Chicago Press, Chicago, 1977). A number of surveys have been carried out since 1988 in the supposed range of S. tripartitus, in both Ecuador and Peru. Here we summarize and discuss these issues and provide a new suggestion for the geographic range of this species; that is, between the ríos Napo and Curaray in Peru and extending east into Ecuador. We also review current evidence for the distributions of Spix's black-mantle tamarin (S. nigricollis nigricollis), Graells' black-mantle tamarin (S. n. graellsi), and the saddleback tamarin (S. fuscicollis lagonotus), which are also poorly known, and examine the evidence regarding sympatry between them. We conclude that despite the existence of a number of specimens with collecting localities that indicate overlap in their geographic ranges, the fact that the four tamarins are [corrected] of similar size and undoubtedly very similar in their feeding habits militates strongly against the occurrence of sympatry among them.     

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.     

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.     

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.     

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.     

Erratum to: The range of the golden-mantle tamarin, <Emphasis Type="Italic">Saguinus tripartitus</Emphasis> (Milne-Edwards, 1878): distributions and sympatry of four tamarins in Colombia,Ecuador, and northern Peru

A detailed understanding of the range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878), in Amazonian Peru and Ecuador is of particular relevance, not only because it is poorly known but also because it was on the basis of its supposed sympatry with the saddleback tamarin (S. fuscicollis lagonotus) that Thorington (Am J Primatol 15:367–371, 1988) argued that it is a distinct species rather than a saddleback tamarin subspecies, as was believed by Hershkovitz (Living new world monkeys, vol I. The University of Chicago Press, Chicago, 1977). A number of surveys have been carried out since 1988 in the supposed range of S. tripartitus, in both Ecuador and Peru. Here we summarize and discuss these issues and provide a new suggestion for the geographic range of this species; that is, between the ríos Napo and Curaray in Peru and extending east into Ecuador. We also review current evidence for the distributions of Spix’s black-mantle tamarin (S. nigricollis nigricollis), Graells’ black-mantle tamarin (S. n. graellsi), and the saddleback tamarin (S. fuscicollis lagonotus), which are also poorly known, and examine the evidence regarding sympatry between them. We conclude that despite the existence of a number of specimens with collecting localities that indicate overlap in their geographic ranges, the fact that the four tamarin species are of similar size and undoubtedly very similar in their feeding habits militates strongly against the occurrence of sympatry among 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.