Proposed nutritional importance of plant exudates in the diet of the Panamanian Tamarin,Saguinus oedipus geoffroyi

Data collected on the feeding behavior of Saguinus oedipus geoffroyi(Panamanian tamarin) in Panama show that plant exudates, as well as insects and fruits, are a major component of the diet. During the months of May, June, and July, tamarins were observed clinging to the trunks of Anacardium excelsum(Anacardiaceae) while feeding on exudates. These observations accounted for greater than 14% of the total feeding time of this primate. Nutritional analyses indicate that Anacardiumexudates provide these tamarins with a rich source of the mineral calcium as well as protein, carbohydrates, and water. The seasonal pattern of exudate feeding observed in S. oedipusappears to coincide with certain nutritionally sensitive periods of the reproductive cycle and may serve to offset a potential mineral imbalance incurred during the terminal phase of gestation and lactation.     

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.     

Intracardiac thrombosis and aortic dissecting aneurysms in mustached tamarins (Saguinus mystax) with cardiomyopathy

Spontaneous intracardiac thrombosis is rarely reported in animals, particularly nonhuman primates. The finding of 2 cases of intracardiac thrombi in mustached tamarins (Saguinus mystax) that died as a consequence of congestive heart failure prompted us to do a retrospective study to determine the frequency of this condition. Clinical records, necropsy reports, and tissues from 60 mustached tamarins that died or were euthanized between 1996 and 2009 were reviewed. Of the 60 monkeys whose cases were reviewed, 10 (16.6%) had intracardiac thrombi, and 4 (6.6%) had dissecting aortic aneurysms. Of the 10 animals with intracardiac thrombosis, 3 had left ventricular involvement alone; 4 monkeys had thrombi only in the right ventricle, and the remaining 3 animals exhibited thrombi in both ventricles. Myocardial fibrosis and chronic renal disease were common findings in affected animals. The causes of the intracardiac thrombosis in the tamarins in the present study are not known, but the clinical signs and gross and microscopic lesions suggest that congestive heart failure secondary to cardiomyopathy is the primary contributor. In addition, the cause of the aortic dissecting aneurysms in the tamarins in this study is not known. Further studies are required to determine whether factors including aortic curvature, genetic background, or hypertension-alone or in combination-play a role. To our knowledge, the current retrospective study is the first report of intracardiac thrombosis and aortic aneurysms in mustached tamarins.     

Geophagy in moustached tamarins,Saguinus mystax (platyrrhini: Callitrichidae), at the Río Blanco,Peruvian Amazonia

During a field study at the Río Blanco in northeastern Peru between June and September 1990, moustached tamarins (Saguinus mystax) were observed to feed on soil material on three different occasions. Soil was taken directly from bare spots of surface soil (two observations) and from the broken mound of leaf-cutting ants (Atta sp.; one observation). Exposed surface soil is rare throughout the study area. Geochemical analyses of the soils that were consumed showed elevated concentrations of several elements in the ant mound sample compared to the other two soil samples. The most likely hypothesis for the function of soil feeding in moustached tamarins is that it serves in mineral supplementation.     

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

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

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.     

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.     

Temperature-metabolism relations in the cotton-top tamarin (Saguinus oedipus) model for ulcerative colitis

Examination of temperature-metabolism relations found no significant differences between thermoregulation of temperature housed laboratory cotton-top tamarins (Saguinus oedipus) and wild tamarins in Colombia, S.A. The results indicate that tamarins do not acclimate to a temperate environment and are metabolically stressed at T_a less than 32°C. This is consistent with an hypothesis of chronic metabolic stress as a factor in the etiology of cotton-top tamarin colitis, which is restricted to captive populations and not found in wild tamarins.     

Chromosomal similarities and differences between tamarins,Leontopithecusand Saguinus (Platyrrhini,Primates)

The karyotypes of two taxa of genus Leontopithecus(rosalia and chrysomelas) are studied. Their G-, C- and NOR-banding patterns are compared with those of representatives of the genus Saguinus to determine chromosomal similarities and differences between the two genera and thus contribute to explaining phylogenetic relations between the tamarins. Leontopithecus, like the Saguinus, presents 2n = 46, 14 autosomes plus the Y acrocentric and 30 autosomes plus the X biarmed. No chromosomal rearrangement distinguishes the karyotypes of the representatives of genus Leontopithecus or genus Saguinus. The two genera are distinguished from each other by a paracentric inversion and pericentric inversions on at least four pairs of acrocentric autosomes, displacing the NORs of the small short arms in Leontopithecus to the proximal region of the long arms in Saguinus or vice versa. The tamarins are also distinguished by the distribution of noncentromeric constitutive heterochromatin. The data obtained indicate that the two tamarin genera are closely related chromosomally, suggesting that they probably originated from the same ancestral branch. Am. J. Primatol. 43:265–276, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

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.     

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.     

Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax)

In several primate taxa there is evidence that the social and physical environment can exert a significant effect on reproductive behavior and biology. In this paper we examine social and physiological factors influencing group composition and reproduction in free-ranging moustached tamarin monkeys (Saguinus mystax mystax). This species is characterized by cooperative care of the young and a breeding system that includes both polyandrous and polygyandrous matings. Body measurements collected on adult males residing in multimale groups indicate marked within-group differences in testes volume. In 12 of 17 groups examined, testes volume of at least two resident adult males differed by 21–174%. Among these males, testes volume was not correlated with either body weight or adult age class. We also examine whether factors such as time of year had an effect on reproductive condition. An analysis of body measurements of 128 adult male and 127 adult female moustached tamarins, wild-trapped and released in northeastern Peru, indicates cyclic changes in genital size. For males, mean monthly testes volume in July (712 mm³) was twice that recorded in June (351 mm³). Females exhibited a similar pattern. Although endocrine information on intra- and intersexual social effects on fertility are unavailable for S. mystax, given the high degree of social cooperation and lack of overt aggression among adult male group members, we offer the possibility that resident male moustached tamarins compete for access to the groups' lone breeding female through socially induced reproductive suppression and sperm competition. © 1996 Wiley-Liss, Inc.     

Captive cotton‐top tamarins' (Saguinus oedipus oedipus) use of landmarks to localize hidden food items

Seventeen captive cotton‐top tamarins (Saguinus oedipus oedipus) were individually tested on their use of spatial relationships between landmarks to locate multiple hidden food items. In two experiments, the tamarins were presented with a spatial‐foraging task in which positions of hidden food rewards were fixed in relation to an array of visual cues. In Experiment 1, the cues+hidden food configuration was rotated 90° and the tamarins were successful in locating the food items significantly above chance levels (P<0.01). In Experiment 2 the cues+hidden food configuration was translated (up, down or sideways) from the previously learned configuration, and the monkeys successfully localized the hidden food items (P<0.001). Results indicate that the tamarins relied on the spatial relationship between the multiple landmarks to locate hidden food items rather than on an associative or beacon strategy. The results of these experiments support the contention that when contextually appropriate these captive New World monkeys have the capacity to rely on the spatial relationship or positions of several cues as an array to localize points in their environment. Am. J. Primatol. 71:316–323, 2009. © 2009 Wiley‐Liss, Inc.     

Locomotor behavior and feeding ecology of the panamanian tamarin (Saguinus oedipus geoffroyi,callitrichidae, primates)

The Callitrichidae are a family of New World primates that exhibit a complex of behavioral and morphological characters reputedly similar to those of tree squirrels of the genus Sciurus.In particular, the locomotor behavior of tamarins and marmosets has been described as “squirrel-like. ” In this paper I describe a field investigation of the locomotor behavior and ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi)and the redtailed squirrel (Sciurus granatensis).From January through August 1978, a total of 1200 hr was spent observing freeranging populations of tamarins and tree squirrels in an area of secondary forest on the Pacific Coast of Panama. Observations were made using an instantaneous time sampling technique. Individual activity records were collected on focal animals and recorded at 2.5-min intervals throughout the day. The following information was collected: (a) nature and structure of the substrate exploited, (b) activities on these supports and/or types of resources procured, and (c) body posture involved in the use of these supports. Data presented indicate major differences in substrate preference and positional behavior in tamarins and tree squirrels. Unlike squirrels, tamarins avoid vertical and sharply inclined supports during travel. Movements through the canopy is accomplished by a series of long leaps which begin and end on thin terminal supports. However, the Panamanian tamarin spent numerous hours clinging to large vertical trunks while feeding on plant exudate. Gums comprise 23.O% of the noninsect portion of the tamarin diet. The relationships between small body size, claw-like nails, substrate preference, and positional behavior are discussed. Claw-like nails enable this primate to exploit a food resource that would otherwise be inaccessible. The interrelationship between environment, behaviour, and morphology provides a frameworks from which to understand callitrichid adaptations. These adaptations are not convergent with those of the sciurid rodents. An earlier draft of this paper was presented at the 48th Annual Meeting of the American Association of Physical Anthropologists, San Francisco, April 1979.     

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins

The establishment of baseline data on parasites from wild primates is essential to understand how changes in habitat or climatic disturbances will impact parasite–host relationships. In nature, multiparasitic infections of primates usually fluctuate temporally and seasonally, implying that the acquisition of reliable data must occur over time. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over 3 years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explored variation in parasite prevalence across age and sex classes, test nonrandom associations of parasite co‐occurrence, and assess the relationship between group size and PSR. From 288 fecal samples across 105 individuals (71 saddleback and 34 emperor tamarins), 10 parasite taxa were identified by light microscopy following centrifugation and ethyl‐acetate sedimentation. Of these taxa, none were host‐specific, Dicrocoeliidae and Cestoda prevalences differed between host species, Prosthenorchis and Strongylida were the most prevalent. Host age was positively associated with Prosthenorchis ova and filariform larva, but negatively with cestode and the Rhabditoidea ova. We detected no differences between expected and observed levels of co‐infection, nor between group size and parasite species richness over 30 group‐years. Logistic models of individual infection status did not identify a sex bias; however, age and species predicted the presence of four and three parasite taxa, respectively, with saddleback tamarins exhibiting higher PSR. Now that we have reliable baseline data for future monitoring of these populations, next steps involve the molecular characterization of these parasites, and exploration of linkages with health parameters.     

Factors Affecting Group Spread within Wild Mixed-Species Troops of Saddleback and Mustached Tamarins

We examined group spread and interindividual spacing within wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Mustached tamarin groups were spread over larger areas than those of saddleback tamarins. Group size and behavior affected group spread and interspecific proximity: larger groups of both species were dispersed over greater areas, and the larger troop had the lowest degree of interspecific proximity. Behavior also affected group spread and interspecific proximity: when traveling individuals were spread over a larger area, and the distance between heterospecifics was greater than when stationary. We examined spatial proximity using data on the distance from nearest neighbor. Overall, distance to nearest neighbor was not affected by group size. Based on specific behaviors, foraging saddleback tamarins were significantly nearer conspecifics than to mustached tamarins. Tamarins have polymorphic color vision, and trichromats—having 3 types of visual pigment—versus dichromatic individuals—with two types of pigment—may be better at perceiving yellow or russet colored predators and conspecifics than their dichromatic counterparts are. Color vision status affected spatial positioning, with vigilant trichromats being further from their neighbors than their dichromatic conspecifics were. We discuss the findings with respect to the ecology of the species. Specifically, interspecific differences in group spread and spatial proximity are related to differences in the supports used, and the effect of troop size on interspecific proximity is related to increased resource competition. The finding that trichromats are further from their neighbors represents the first example of a behavioral correlate of color vision ability in a wild species with polymorphic color vision, and is explained through the perception of predation risk.     

Changes in the activity of captive cotton-top tamarins (Saguinus oedipus) over the breeding cycle

The energetic costs of reproduction are likely to be particularly high in the Callitrichidae (marmosets and tamarins), which characteristically produce twin litters. The activity of five captive breeding pairs of cotton-top tamarins (Saguinus oedipus) was investigated for a 6-month period covering the second half of pregnancy and lactation. Breeding males showed few major changes in activity over this period, but breeding females reduced their levels of locomotion during late pregnancy, and during lactation they spent up to twice as much time feeding and foraging as they did during pregnancy. These results support the hypothesis that the costs that callitrichid females incur when reproducing are likely to have been an important factor in the evolution of these species' communal rearing systems.     

High‐throughput sequencing of fecal DNA to identify insects consumed by wild Weddell's saddleback tamarins (Saguinus weddelli,Cebidae, Primates) in Bolivia

The genus Saguinus represents a successful radiation of over 20 species of small‐bodied New World monkeys. Studies of the tamarin diet indicate that insects and small vertebrates account for ～16–45% of total feeding and foraging time, and represent an important source of lipids, protein, and metabolizable energy. Although tamarins are reported to commonly consume large‐bodied insects such as grasshoppers and walking sticks (Orthoptera), little is known concerning the degree to which smaller or less easily identifiable arthropod prey comprises an important component of their diet. To better understand tamarin arthropod feeding behavior, fecal samples from 20 wild Bolivian saddleback tamarins (members of five groups) were collected over a 3 week period in June 2012, and analyzed for the presence of arthropod DNA. DNA was extracted using a Qiagen stool extraction kit, and universal insect primers were created and used to amplify a ～280 bp section of the COI mitochondrial gene. Amplicons were sequenced on the Roche 454 sequencing platform using high‐throughput sequencing techniques. An analysis of these samples indicated the presence of 43 taxa of arthropods including 10 orders, 15 families, and 12 identified genera. Many of these taxa had not been previously identified in the tamarin diet. These results highlight molecular analysis of fecal DNA as an important research tool for identifying anthropod feeding patterns in primates, and reveal broad diversity in the taxa, foraging microhabitats, and size of arthropods consumed by tamarin monkeys. Am J Phys Anthropol 156:474–481, 2015. © 2014 Wiley Periodicals, Inc.