Saguinus Fuscicollis Research Articles

Adrenal cortical epithelial cysts in two saddleback tamarins ( Saguinus fuscicollis)

Adrenal cysts of epithelial origin were found incidentally in the adrenal cortical tissues of two adult female saddleback tamarins. In one case, a small cluster of minor cysts was located at the cortico-medullary border. The cysts were filled with a periodic acid-Schiff (PAS)-positive, amorphous substance and lined by a cuboidal PAS-negative epithelium, which resembled morphologically the ascending Henle's loops of the kidney. These microcysts were thought to be mesonephric remnants. In the second case, two large cysts of 1 to 3 mm diameter extended throughout the entire cortex. The cysts were filled by a watery, PAS-negative fluid and lined by a bi- to multi-layered, cytokeratin-positive epithelium. The basal epithelial layer consisted of cuboidal cells, which became cylindrical to drop-like in appearance towards the cyst lumen. The cysts closely resembled mesothelium-derived adrenal cysts in man. This is the first report of adrenal cysts in non-human primates.

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.

Exhibiting mixed-species groups of sympatric tamarins Saguinus spp at Belfast Zoo

In the wild sympatric tamarin species show a high degree of spatial co-ordination. Stable associations between Saddleback tamarins Saguinus fuscicollis and members of the Saguinus mystax group (Red-bellied tamarin Saguinus labiatus, Emperor tamarin Saguinus imperator and Moustached tamarin S. mystax) have been observed at all sites where the species co-occur and are related to the stratification of ecological niches within the forest. Since 1992 a study of mixed-species tamarin groups has been carried out at Belfast Zoo. Stable associations were established between groups of S. labiatus and S. fuscicollis, and few agonistic interactions were observed. Most aggression involved disputes over food and typically consisted of S. labiatus displacing S. fuscicollis, merely by approaching. Other interactions included some inter-specific grooming and huddling. This paper describes the introduction procedure and the social and reproductive behaviour of each species within the group, and suggests that mixed-species exhibits may be a beneficial way of exhibiting tamarins.

Food patch structure and plant resource partitioning in interspecific associations of amazonian tamarins

Avila-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.

Riverine barriers and gene flow in Amazonian saddle-back tamarins.

We describe patterns of genotypic and phenotypic variation in saddle-back tamarin (Saguinus fuscicollis) populations along the central and upper Rio Juruá, western Brazilian Amazonia. The genetic data are sequence haplotypes of the mitochondrial cytochrome b gene; phenotypic data are pelage colour variants that define sharply demarcated subspecies of this extremely variable tamarin species. We show that gene flow occurs between adjacent subspecies, but that this phenomenon is restricted to the headwater section of the river, which is consistent with expectations from the riverine barrier hypothesis. In this model, the major first-order tributaries of the Amazon form effective barriers to dispersal, with between-bank gene flow limited to the narrowed sections of headwater streams and parallel divergence increasing along both banks from the headwaters to the mouth of a given river. In meandering rivers such as the Rio Juruá, we suggest passive transfer through river channel dynamics as the main mechanism permitting genetic contact between populations on opposite banks of the river. Finally, we argue that in the case of plant and animal species that are largely restricted to unflooded (terra firme) forests, such as tamarins, seasonally flooded (várzea) forest can operate as a critical additional barrier to between-bank gene flow.

Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: Evidence from a thirteen-year study of a marked population

We monitored a population of four to seven groups of individually marked saddle-back tamarins (Saguinus fuscicollis; Callitrichidae) at the Cocha Cashu Biological Station in Peru's Manu National Park every year from 1979 through 1992. In this paper we use data on life histories, group compositions, group formations, and dispersal patterns collected during these 13 years to examine the reproductive strategies of males and females. Group compositions and mating patterns were quite variable in this population, with both monogamy and cooperative polyandry common. In polyandrous groups, two males shared a female's copulations and cooperatively cared for her young. Although most groups contained a single breeding female, we recorded four cases in which secondary females successfully reared young. Most young females appeared to wait in their natal groups for the first opportunity to fill a primary breeding position in their own or a neighboring group. Females that acquired primary breeding positions maintained those positions for a mean of 3 years. No female was observed to transfer between groups a second time. Variation in female lifetime reproductive success was high. Half of the females marked as juveniles never bred; the other half produced an average of 3.5 young. A paucity of female breeding opportunities may explain the high mortality of females between 2.5 and 4.5 years of age and the resulting male-biased adult sex ratio. The majority of groups contained more than one probable male breeder. Polyandrous groups included both related and unrelated males. Behavioral differences between Cocha Cashu tamarins and other studied populations may result from the pressures of living in an environment inhabited by nine other primate species and numerous predators. © 1996 Wiley-Liss, Inc.

Birth seasonality in cotton-top tamarins (saguinus oedipus) despite constant food supply and body weight

Goldizen et al. (1988) reported that wild saddle-back tamarins (Saguinus fuscicollis, Callitrichidae) show birth seasonality that is correlated with food supply and body weight. They suggested a sequence of ultimate causality in which shortage of food leads to reduced body weight which leads to timing of weaning and lactation when resources are more abundant. Cotton-top tamarins in captivity show birth seasonality despite constant food supply and body weight. Although natural availability of fruit and insects (which are key foods for tamarins) is related to rainfall, birth seasonality and body weight in captive cotton-top tamarins are unrelated to rainfall. The most likely proximate mechanism for seasonality of births in tamarins is photo-period, given existing data on populations living in natural and artificial lighting.

Morphological Integration in the Saddle-Back Tamarin (Saguinus fuscicollis) Cranium

Quantitative genetic theory predicts that functionally and developmentally related characters will be morphologically integrated and tend to be inherited together. Furthermore, coinheritance and environmental integration of functionally related characters may be important in facilitating adaptive evolution. The hypothesis that functionally and developmentally related features of the cranium are phenotypically, genetically, and environmentally integrated in the saddle-back tamarin (Saguinus fuscicollis) cranium is tested. Thirty-nine craniofacial measurements were taken on 209 animals from the Oak Ridge Associated Universities' Marmoset Research Center. Heritabilities and phenotypic, genetic, and environmental correlations were calculated using maximum likelihood methods after the data were corrected for sex and specified environmental effects. The correlation matrices were compared to a series of theoretical intertrait connectivities representing expected patterns of morphological integration using Mantel's test. The patterns of phenotypic, genetic, and environmental correlation among craniofacial traits matched patterns predicted on the basis of developmental and functional relationships among cranial traits. The similarity between functional and developmental integration and correlation was largely due to the relatively high correlations among cranial vault traits and among oral traits. Both genetic and environmental correlation among developmentally and functionally related characters may enhance the rate of evolutionary change.

Endocrine monitoring of the ovarian cycle and pregnancy in the saddle-back tamarin (Saguinus fuscicollis) by measurement of steroid conjugates in urine.

Direct measurements of urinary immunoreactive estrone conjugates (E1C) and pregnanediol glucuronide (PdG), were applied to monitoring the ovarian cycle (n = 9) and pregnancy (3 full term pregnancies, 2 mid-term abortions) in Saguinus fuscicollis. During the ovarian cycle, urinary E1C concentrations revealed a high degree of day-to-day variability and appeared to be uninformative in reflecting cyclic ovarian function. In contrast, PdG was a reliable indicator of ovarian cyclicity with excretion patterns corresponding well with plasma progesterone profiles. Luteal phase PdG concentrations were on average 4-7-fold higher than corresponding follicular phase values. On the basis of changes in circulating progesterone, a mean cycle length of 25.7 ±1.0 days with an average follicular phase of 7.1 ± 0.6 days and a mean luteal phase of 18.6 ± 0.7 days, was found (n = 14 cycles). Following conception, both urinary steroid conjugate concentrations increased and elevated levels were maintained beyond the normal luteal phase length, allowing pregnancy to be determined at around day 25-30. During mid- to late pregnancy, PdG levels declined while E1C concentrations continued to be elevated until approximately 6 weeks before parturition when a decrease occurred. Both hormones showed a clear and rapid fall to follicular phase values following termination of pregnancy at either parturition or mid-term abortion. Post partum ovulations (n = 5) occurred on average 17-18 days following birth with four ovulations leading to conceptions. The results demonstrate the potential of urinary steroid conjugate analysis as a practical and reliable method for non-invasive monitoring of reproductive status in the female saddle-back tamarin. © 1995 Wiley-Liss, Inc.

Primate Responses to Phenological Changes in an Amazonian Terra Firme Forest

The responses of saddleback tamarins Saguinus fuscicollis avilapiresi, moustached tamarins S. mystax pileatus, brown capuchins Cebus apella and gray woolly monkeys Lagothrix lagotricha cana to seasonal changes in plant phenology were examined in undisturbed terra firme forest in the upper Urucu river, Brazilian Amazonia. Primate species fed largely on ripe fruit pulp for most of the year, but shifted to alternative plant resources during the dry season, when the density of fruiting trees and the abundance of ripe fruit reached their lowest levels. The main dry season plant resource used by the two tamarin species was nectar, while those of brown capuchins and woolly monkeys are immature seeds and young foliage, respectively. Exudates of Parkia seedpods were heavily used by all species. Nondietary seasonal adaptations to lean fruit supplies are described for these and other sympatric primate species mainly in terms of pronounced shifts in habitat use and ranging behavior. -from Author

Evidence of hybrid vigor in subspecific hybrids of the saddle-back tamarin (Saguinus fuscicollis).

The effect of hybridization on infant survival was investigated in subspecific crosses of the saddle-back tamarin (Saguinus fuscicollis) at the Oak Ridge Associated Universities (ORAU) Marmoset Research Center (Oak Ridge, TN). Cox Proportional Hazards Regression was used to compare infant survival between (1) pure subspecies, (2) F1, F2, and backcrossed hybrids, and (3) hybrids and their parental subspecies. Also, effects of management changes, sex, and litter size on infant survival were investigated. There were no significant differences in infant survival between the pure subspecies. Also, degree of hybridization (F1, F2, or backcross) did not have a significant effect on infant survival. Progeny of hybrid crosses between S. f. lagonotus and S. f. illigeri was found to have significantly (P < 0.05) higher infant survival than both of their parental subspecies. Individuals born after diet and management changes in the colony had significantly (P < 0.05) higher survival than those born before. There were no significant sex differences in infant survival. Individuals born into triplet litters had significantly (P < 0.05) lower survival than those born into twin litters. These results show heterosis (hybrid vigor) for infant survival in one subspecific S. fuscicollis cross (S. f. lagonotus × S. f. illigeri). The results suggest genetic divergence between the subspecies populations and possible reproductive isolation in the wild. © 1994 Wiley-Liss, Inc.

Cholesterol metabolism in new world primates: Comparative studies in two tamarin species ( Saguinus oedipus and Saguinus fuscicollis) and the squirrel monkey ( Saimiri sciureus)

1. 1. Cholesterol metabolism has been characterized in three species of New World primates, the cotton-top tamarin, the saddle-back tamarin, and the squirrel monkey. 2. 2. When fed a diet containing cholesterol, the three species exhibited differing responses of plasma cholesterol levels. 3. 3. Dietary cholesterol absorption was determined and plasma cholesterol die-away kinetics were analyzed in terms of a two-pool model. 4. 4. The results of the analyses of cholesterol turnover are consistent with the observed species-specific differences in plasma cholesterol values and cholesterol absorption. 5. 5. Cholesterol metabolism differs between the two tamarin species, as well as between the tamarins and the squirrel monkey. 6. 6. Implications of species-specific differences between tamarin species are discussed in terms of the use of tamarin species as animal models for comparative studies of cholesterol metabolism and the etiology of cancer and cardiovascular disease.

Modeling monkeys: A comparison of computer-generated and naturally occurring foraging patterns in two species of neotropical primates

We present a series of computer-generated foraging models (random movement, olfactory navigation, and spatial memory) designed to examine the manner in which sensory cues and cognitive skills might be used by rainforest monkeys to locate patchily distributed feeding sites. These simulations are compared with data collected in the Amazon Basin of northeastern Peru on the foraging patterns of two species of neotropical primates, the moustached tamarin monkey (Saguinus mystax) and the saddle-back tamarin monkey (Saguinus fuscicollis). The results indicate that, although tamarins may rely on olfactory cues to locate nearby feeding sites, their foraging patterns are better explained by an ability to maintain a detailed spatial map of the location and distribution of hundreds of feeding trees in their home range. There is evidence that such informationis retained for a period of at least several weeks and is used to minimize the distance traveled between widely scattered feeding sites. The use of computer simulations provides a powerful research tool for generating predictive models regarding the role of memory and sensory cues in animal foraging patterns.

Anti-predation benefits in a mixed-species group of Amazonian tamarins.

Because of their small body size, tamarins are potentially vulnerable to a wide range of predator species. This paper examines the general patterns of predator avoidance of the Avila-Pires saddle-back tamarin (Saguinus fuscicollis avilapiresi) and the red-cap moustached tamarin (Saguinus mystax pileatus) in the upper Urucu river, Amazonas, Brazil. One highly stable mixed-species group of these species suffered an average of 1 attack by carnivorous raptors every 8.8 days of activity. Although none of these attacks was successful tamarins occasionally fall prey to raptors or terrestrial predators. The two tamarin species exhibited a high degree of coordination in their anti-predation tactics. Saddle-back tamarins accounted for most of the vigilance and detection of terrestrial and scansorial threats, whereas moustached tamarins scanned for and detected most aerial and arboreal threats. Of the two species, however, moustached tamarins contributed a significantly greater proportion of scanning time after predation attempts, during pre-retirement periods and at other times. Moreover, their substantially larger groups (1.6 times larger than those of saddle-back tamarins) accounted for a further increase in their effective vigilance effort. The anti-predation benefits gained by saddle-back tamarins from joining mixed-species groups with moustached tamarins thus appeared to be greater than the reverse, because the latter provide greater protection to the group, particularly against aerial sources of threat. However, the greater vigilance of saddle-back tamarins towards potential terrestrial predators cannot be discounted, because these may on rarer occasions pose a real threat to either species.(ABSTRACT TRUNCATED AT 250 WORDS)

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.

Genetic differences among subspecies of the saddle-back tamarin (Saguinus fuscicollis):evidence from hybrids.

The subspecies of saddle-back tamarins (Saguinus fuscicollis) are known to be chromatically and morphologically diverse but little is known of the genetic basis for the observed morphological variation. The morphology of first generation subspecific hybrids can be compared to that of the parental subspecies to provide information on the extent and nature of genetic differences in morphology between subspecies. We compare two groups of saddle-back tamarin hybrids (S. f. illigeri × S. f. lagonotus and S. f. illigeri × S. f. leucogenys) to pure-bred members of their parental subspecies. These crosses were examined for heterosis, caused by allele frequency differences between the subspecies in combination with directional dominance. Thirty-nine craniofacial measurements were derived from three-dimensional coordinates of landmarks on 355 adult tamarin skulls. These measurements were corrected for sex differences and differences due to environment (wild-derived vs. laboratory-born) prior to analysis of hybridity. Sex differences were minimal for these traits. Environment had a more significant effect on craniofacial morphology. Laboratory environments produce larger faces but smaller orbits, anterior cranial vaults, and cranial bases. Significant heterosis was found for many individual traits and for the first principal component representing size and size-related shape measurements in the S. f. illigeri × S. f. lagonotus cross. The smaller samples involved in the S. f. illigeri× S. f. leucogenys cross led to a much lower number of statistically significant results, although most traits did display heterosis. Heterosis for craniofacial size was nearly statistically significant. These results suggest that there are large differences in allele frequencies among these subspecies of saddle-back tamarin for genes affecting craniofacial morphology. Based on these data we suggest that these subspecies are likely to be independent, largely isolated, evolutionary units. © 1993 Wiley-Liss, Inc.

Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and S. mystax

Tamarins of the genus Saguinus feed on a wide range of arthropods and small vertebrates, which compose a critical component of their diet. This paper examines the foraging patterns and capture success of the Avila-Peres saddle-back (S. fuscicollis avilapiresi) and the red-capped moustached tamarin (S. mystax pileatus) in very stable mixed-species groups, and whether and how any foraging benefits for either species resulted from their association. Moustached tamarins actively searched for prey items which were mainly well exposed on the midstorey foliage. Saddle-back tamarins, on the other hand, foraged at lower heights, largely by manipulating a variety of microhabitats potentially concealing embedded prey. The foraging activity of the numerically dominant and larger-bodied moustached tamarins often resulted in prey items escaping to lower substrates, usually the forest leaf-litter. The “beating effect” of this species substantially facilitated captures of large, mobile prey items by saddle-backs, which were highly adept at locating and retrieving flushed prey. It is estimated that, while saddle-backs obtained 66–73% of their prey biomass from flushed items, this proportion was substantially lower (2–9%) for moustached tamarins. Commensal insectivory appears to involve a highly asymmetric benefit to saddle-backs, and a low cost to moustached tamarins, which partly explains the stability of mixed-species groups.

Consequences of Joint-Territoriality in a Mixed-Species Group of Tamarin Monkeys

AbstractGroups of saddle-back (Saguinus fuscicollis) as moustached tamarins (Saguinus mystax) in a western Amazonian forest jointly defended home ranges larger than 100 ha, which were held in common throughout the year. Resources were defended by direct exploitation in extensive areas shared with other groups, or through intensive and frequent intergroup interactions along territorial boundaries. These interactions were expressed primarily during intergroup encounters, and affected the use of space, movements, time budget, and foraging success of tamarins. During encounters, animals of both species spent more time in energetically costly activities, such as rapid travel and intergroup chases, and less time in energetically positive activities, such as feeding and foraging. In addition, foraging success per unit of foraging effort within overlapping areas of the range periphery was lower than in exclusive areas of the range centre, particularly for saddle-back tamarins. The time and energy allocated by moustached tamarins to boundary contests was considerably greater than that of saddle-backs, despite the fact that only the latter species increased its foraging efficiency by shifting from exclusive areas in the group's range to those shared by other groups. This is probably because of saddle-back's greater use of depletable food supplies, such as small fruit patches and small microhabitats containing embedded prey items. These benefits are likely to justify the substantial amount of time and energy invested in territorial defence for both saddle-backs and moustached tamarins, but appeared to be highly asymmetric between species.

A field study on the red-bellied tamarin,Saguinus l. labiatus, in Bolivia

A 5-month field study was conducted on red-bellied tamarins,Saguinus labiatus labiatus, in the Pando Department of northern Bolivia. Group sizes ranged from 5 to 10 animals, and each group associated with a group of saddle-backed tamarins,Saguinus fuscicollis weddelli. Members of three groups were trapped and marked and data were collected by radiolocation. The average range size used over 10 days was 19 ha. On average the groups entered about 29% of their range each day and had a mean daily path length of about 1487 m. The groups used a number of different sleeping sites within their ranges. They fed on a variety of different fruits and also on nectar from flowers, resin, and insects. Areas within the home range which were used significantly more than expected were generally those in which one or more of the following existed: a sleeping site, an intergroup encounter site, or a site where the group took shelter during an extended period of heavy rain.

Untersuchungen zur Freßfiaktivität, Spontanaktivität und Körperkerntemperatur von Braunrücken‐Tamarinen (Saguinus fuscicollis)1,2

Eating behaviour and spontaneous activity (videometry) as well as deep body temperature (radiotelemetry) of 3 adult Saddle Back Tamarins (Saguinus fuscicollis) were investigated (singly housed, environmental temperature 28 degrees C, relative air humidity 60%, light 6:00-18:00 h, drinking-water and pelleted colony diet ad lib.). The experimental animals (1 female, 2 males; 3-8 years old), born in captivity, showed only some slight individual differences within their inborn species pattern, with regard to the 3 measured parameters. The monkeys were, like wild-living individuals, strictly light-active. They moved in the day-time nearly uninterrupted without special rhythm and slept remarkably deep through the whole night. Food intake occurred during the whole day with varying intensity. The body temperature of the 3 monkeys showed individual daytime-means between 38.8-39.9 degrees C, whereby the temperature fluctuated dependent on their moving activity with a range of about +/- 0.5 degrees C. At night the body temperature of the animals averaged between 35.9-36.6 degrees C.