Saguinus Mystax Research Articles

Saguinus mystax(Primates: Callitrichidae)

AbstractSaguinus mystax (Spix, 1823), a callitrichid (tamarin and marmoset family) commonly called the mustached tamarin, is 1 of 12 species in the genus Saguinus. In this large callitrichid (450–650 g), females are slightly heavier than males. It occurs in Brazil and Peru, south of Rio Amazonas from Río Ucayali in the west to Rio Purus in the east, in primary and secondary tierra firma rainforests. The diet consists of fruit pulp, insects, gums, nectar, and small vertebrates. It lives in groups of 3–10 individuals with a male-biased adult sex ratio and has a cooperative breeding system. In areas of sympatry, S. mystax forms mixed-species groups with saddle-back tamarins, Leontocebus. Although captured for the pet trade and sporadically hunted, it is considered “Least Concern” (LC) by the International Union for Conservation of Nature.

Five novel bifidobacterial species isolated from faeces of primates in two Czech zoos: Bifidobacterium erythrocebi sp. nov., Bifidobacterium moraviense sp. nov., Bifidobacterium oedipodis sp. nov., Bifidobacterium olomucense sp. nov. and Bifidobacterium panos sp. nov.

Five Bifidobacterium strains, VB23T, VB24T, VB25T, VB26T and VB31T, were isolated from chimpanzee (Pan troglodytes), cotton-top tamarin (Saguinus oedipus), Goeldi's marmoset (Callimico goeldii), moustached tamarin (Saguinus mystax) and patas monkey (Erythrocebus patas), respectively, which were kept in two Czech zoos. These strains were isolated from faecal samples and were Gram-positive, non-motile, non-sporulating, anaerobic and fructose-6-phosphate phosphoketolase-positive. Phylogenetic analyses based on 16S rRNA revealed close relatedness between VB23T and Bifidobacterium angulatum LMG 11039T (96.0 %), VB24T and Bifidobacterium pullorum subsp. pullorum DSM 20433T (96.1 %), VB25T and Bifidobacterium goeldii LMG 30939T (96.5 %), VB26T and Bifidobacterium imperatoris LMG 30297T (98.1 %), and VB31T and B. angulatum LMG 11039T (99.40 %). Internal transcribed spacer profiling revealed that VB23T, VB24T, VB25T, VB26T and VB31T had highest similarity to Bifidobacterium breve LMG 13208T (77.2 %), Bifidobacterium longum subsp. infantis ATCC 15697T (85.8 %), Bifidobacterium biavatii DSM 23969T (76.9 %), B. breve LMG 13208T (81.2 %) and B. angulatum LMG 11039T (88.2 %), respectively. Average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) analyses with their closest neighbours supported the independent phylogenetic positions of the strains with values between 86.3 and 94.3 % for ANI and 25.8 and 54.9 % for dDDH. These genomic and phylogenetic analyses suggested that the evaluated strains were novel Bifidobacterium species named Bifidobacterium erythrocebi sp. nov. (VB31T=DSM 109960T=CCUG 73843T), Bifidobacterium moraviense sp. nov. (VB25T=DSM 109958T=CCUG 73842T), Bifidobacterium oedipodis sp. nov. (VB24T=DSM 109957T=CCUG 73932T), Bifidobacterium olomucense sp. nov. (VB26T=DSM 109959T=CCUG 73845T) and Bifidobacterium panos sp. nov. (VB23T=DSM 109963T=CCUG 73840T).

Salivary gland neoplasms in non-human primates: A case series and brief literature review.

Salivary gland neoplasms are rare in non-human primates. Thirty-five years of pathology records were reviewed at the Southwest (SNPRC) and Yerkes (YNPRC) National Primate Research Centers. An in-depth literature search for salivary gland neoplasms in non-human primates was performed. Seventeen salivary gland neoplasms (nine from SNPRC and YNPRC, eight from published literature) were identified. There were seven malignant, nine benign, and one of undetermined behavior identified in eight rhesus macaques, six baboons, a chimpanzee, a bonnet macaque, and a moustached tamarin. Parotid gland was the most frequent origin (n=7), followed by mandibular (n=4) or minor salivary glands (n=2). Two animals with salivary gland adenoma had a history of prior radiation exposure. Parotid glands are the most common origin for salivary gland neoplasms. Salivary gland neoplasms should be considered in the differential diagnoses of head and neck masses in non-human primates.

Seasonal variation and an “outbreak” of frog predation by tamarins

We report temporal variation and an "outbreak" of frog predation by moustached tamarins, Saguinus mystax, in north-eastern Peruvian Amazonia. Frog predation rates were generally very low, but strongly increased in October 2015. Other high rates, identified by outlier analyses, were also observed in September-November of other years. Over all study years, predation rates in this 3-month period were significantly higher than those in the remainder of the year, suggesting a seasonal pattern of frog predation by tamarins. Reduced fruit availability or increased frog abundance or a combination of both may be responsible for both the seasonal pattern and the specific "outbreak" of frog predation.

A failed immigration attempt by a moustached tamarin, <i>Saguinus mystax</i>

No abstract

Merkel Cell Polyomavirus Infection of Animal Dermal Fibroblasts.

Merkel cell polyomavirus (MCPyV) is the first polyomavirus to be associated with human cancer. Mechanistic studies attempting to fully elucidate MCPyV's oncogenic mechanisms have been hampered by the lack of animal models for MCPyV infection. In this study, we examined the ability of MCPyV-GFP pseudovirus (containing a green fluorescent protein [GFP] reporter construct), MCPyV recombinant virions, and several MCPyV chimeric viruses to infect dermal fibroblasts isolated from various model animals, including mouse (Mus musculus), rabbit (Oryctolagus cuniculus), rat (Rattus norvegicus), chimpanzee (Pan troglodytes), rhesus macaque (Macaca mulatta), patas monkey (Erythrocebus patas), common woolly monkey (Lagothrix lagotricha), red-chested mustached tamarin (Saguinus labiatus), and tree shrew (Tupaia belangeri). We found that MCPyV-GFP pseudovirus was able to enter the dermal fibroblasts of all species tested. Chimpanzee dermal fibroblasts were the only type that supported vigorous MCPyV gene expression and viral replication, and they did so to a level beyond that of human dermal fibroblasts. We further demonstrated that both human and chimpanzee dermal fibroblasts produce infectious MCPyV virions that can successfully infect new cells. In addition, rat dermal fibroblasts supported robust MCPyV large T antigen expression after infection with an MCPyV chimeric virus in which the entire enhancer region of the MCPyV early promoter has been replaced with the simian virus 40 (SV40) analog. Our results suggest that viral transcription and/or replication events represent the major hurdle for MCPyV cross-species transmission. The capacity of rat dermal fibroblasts to support MCPyV early gene expression suggests that the rat is a candidate model organism for studying viral oncogene function during Merkel cell carcinoma (MCC) oncogenic progression.IMPORTANCE MCPyV plays an important role in the development of a highly aggressive form of skin cancer, Merkel cell carcinoma (MCC). With the increasing number of MCC diagnoses, there is a need to better understand the virus and its oncogenic potential. However, studies attempting to fully elucidate MCPyV's oncogenic mechanisms have been hampered by the lack of animal models for MCPyV infection. To pinpoint the best candidate for developing an MCPyV infection animal model, we examined MCPyV's ability to infect dermal fibroblasts isolated from various established model animals. Of the animal cell types we tested, chimpanzee dermal fibroblasts were the only isolates that supported the full MCPyV infectious cycle. To overcome the infection blockade in the other model animals, we constructed chimeric viruses that achieved robust MCPyV entry and oncogene expression in rat fibroblasts. Our results suggest that the rat may serve as an in vivo model to study MCV oncogenesis.

Mucinous Cystadenoma in the Lung of a Captive-born Moustached Tamarin (Saguinus mystax)

A 2-year-old, captive-born, male moustached tamarin was subjected to necropsy examination after a fatal head trauma. A solitary, circumscribed, subpleural mass (0.6 cm diameter) was found in the right caudal lung lobe. The mass was diagnosed as a mucinous cystadenoma. Histochemical and immunohistochemical tests were performed to further characterize the tumour. Surfactant proteins A, B, C and D were not found in the neoplastic cells, suggesting that the tumour arose from a non-surfactant-producing alveolar lining cell. Pulmonary mucinous cystadenomas are uncommon benign tumours in man and have not been reported previously in animals.

A wild tamarin without a foot— survival despite a handicap

No abstract

A molecular phylogeny of the tamarins (genusSaguinus) based on five nuclear sequence data from regions containingAluinsertions

This study presents a molecular phylogeny of the Saguinus genus, based on the analysis of the DNA sequences of five nuclear loci with Alu insertions in 10 species. The concatenated alignment produced a polytomic arrangement with four main groups, although only two clades-the Amazonian (S. midas, S. niger, and S. bicolor) and the Colombian (S. leucopus and S. oedipus) tamarins-were statistically significant. The emergence of the midas-bicolor clade was estimated at about 5 million years ago (mya), and that of the Colombian clade, at 4.6 mya. The phylogenetic relationships among the mustached tamarins (S. mystax, S. imperator, and S. labiatus) remained unresolved, as did the internal arrangement of the midas group. The lack of a clear consensus on the phylogeny of this group may be related to rapid bursts of evolutionary change within the context of a highly dynamic environment, which may be difficult to resolve using the available quantitative approaches. On the other hand, the discrepancies between mtDNA and nDNA in resolving phylogenies strongly indicate the role of reticulated evolution in the evolutionary history of this group. We hope that the advance of whole genome sequencing technology and increasing information on nuclear markers and SNPs, coupled with a better understanding of the geological phenomena that took place in western Amazonia over the past 20 million years, will shed further light on the phylogenetic history of these New World primates.

The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (Saguinus fuscicollis)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.Electronic supplementary materialThe online version of this article (doi:10.1007/s10764-011-9516-9) contains supplementary material, which is available to authorized users.

Reproductive failure, possible maternal infanticide, and cannibalism in wild moustached tamarins, Saguinus mystax.

Maternal infanticide in wild non-human primates has only been reported twice. In this paper, we report a possible new case of infanticide and cannibalism within a series of four successive reproductive failures in wild moustached tamarins, Saguinus mystax. Necropsy and genetic analyses of the corpses enabled us to rule out any pathology, and to determine paternity. The mother was seen biting and then eating the head of its own infant during a period when another female was pregnant and gave birth just 1 month later. Before that, the perpetrator had given birth to twins three times successfully when four to five adult and subadult males were present in the group. Although we do not know for certain that the infant was alive when the mother started biting it, our field observations preceding the event suggest it probably was. The possible infanticide case and the two cases of births and early death of the infants occurred while only two to three adult males were present in the group. This could be the second case of maternal infanticide reported in the genus Saguinus and the similar circumstances suggest a common pattern. We discuss these events in the light of the different functional explanations of infanticide and conclude that parental manipulation was the most likely: the mother could have terminated the investment in offspring that had low chances of survival in a group with low availability of helpers.Electronic supplementary materialThe online version of this article (doi:10.1007/s10329-011-0238-6) contains supplementary material, which is available to authorized users.

Functions of Intermittent Locomotion in Mustached Tamarins (Saguinus mystax)

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.

Vigilance in a Cooperatively Breeding Primate

Collective vigilance is considered a major advantage of group living in animals. We investigated vigilance behavior in wild mustached tamarins (Saguinus mystax), small, arboreal, cooperatively breeding New World primates that form stable mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We aimed 1) to investigate whether vigilance patterns change according to individual activity and 2) to examine whether there is a social component of vigilance in their cooperative and nonaggressive society. We studied 11 factors that may influence vigilance and used this data to interpret the possible functions of vigilance. We observed 44 individuals in 3 mixed-species and 2 single-species groups of 2 populations that differed in population density and home range sizes. Vigilance changed greatly when individuals were engaged in different activities and individual vigilance was affected by different sets of factors depending on the activity. As vigilance decreased in proximity of conspecifics and heterospecifics when feeding, and in larger mixed-species groups when resting, we conclude that the predominant function of vigilance in mustached tamarins is predator related. However, the absence of the group size effect in very large single-species groups suggests that it may also function to maintain group cohesion. In the population with higher density and smaller home ranges individuals also increased their vigilance in home range overlap areas. We found no evidence that mustached tamarins monitor group mates to avoid food stealing or aggression. The effect of heterospecifics on individual vigilance suggests that collective vigilance might have been an important incentive in the evolution of tamarin mixed-species groups.

The influence of human settlements on the parasite community in two species of Peruvian tamarin

Although there is a growing recognition that the transfer of diseases between humans and non-human primates can be of great significance for conservation biology, there have been only a few studies focusing on parasites. In this study, saddleback (Saguinus fuscicollis) and moustached tamarin (Saguinus mystax) from the rainforest of the Peruvian lowlands were used as models to determine helminth parasite associations between canopy-dwelling primate species and a nearby human settlement. The human population showed high prevalences of infestation with a number of nematodes, including Ascaris lumbricoides (88.9%), Trichuris trichiura (37%) and hookworms (55.6%). However, the ova of these geohelminths were not detectable in tamarin faeces. Thus, no direct parasite transfer from humans to non-human primates could be documented. However, tamarin groups with more frequent contact to humans and their facilities had significantly higher prevalences and egg output of Prosthenorchis elegans, an important primate pathogen, than a forest group. In contrast, a cestode was significantly more common with more egg output in sylvatic than in human-associated groups. Human alteration of the habitat is likely to play a major role in determining the occurrence, prevalence and intensity of helminth infestation of wild non-human primates.

Vigilance of mustached tamarins in single-species and mixed-species groups-the influence of group composition.

Species that participate in mixed-species groups (MSG) may have complementary roles in antipredator strategies. We studied vigilance in mustached tamarins (Saguinus mystax), small arboreal primates that form stable mixed-species groups with saddleback tamarins (Saguinus fuscicollis), in order to examine how the direction of vigilance changes with different species group compositions and whether the division of labor between the two species can be confirmed. We did so by comparing quantitative and qualitative differences in vigilance behavior between same individuals in and out of association (case A); MSG and single-species groups of the same total group size from two different populations (case B); and MSG of the same group size but with a different ratio of conspecifics to heterospecifics (case C). We predicted that individuals would increase downward scanning when heterospecifics are absent or their percentage is low, but total vigilance would increase only in case A due to the group size effect. However, mustached tamarins increased total vigilance due to horizontal scanning in cases A and C, and the predictions were confirmed only in small-sized groups in case B. Thus, we found indications that associating tamarin species in MSG might complement each other in the direction of vigilance, but the division of labor alone does not satisfactorily explain all the findings. There appear to be other mechanisms at work that define how direction of vigilance changes with group size and species composition. Complementarity of species probably occurs due to species vertical stratification rather than differences in the direction of vigilance.

Long‐term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): Effects of foraging, thermoregulation, predation, and resource defense constraints

Sleeping sites are an important aspect of an animal's ecology given the length of time that they spend in them. The sleep ecology of wild saddleback and mustached tamarins is examined using a long-term data set covering three mixed-species troops and 1,300+ tamarin nights. Seasonal changes in photoperiod accounted for a significant amount of variation in sleeping site entry and exit times. Time of exit was more closely correlated with sunrise than time of entry was with sunset. Both species entered their sleeping sites when light levels were significantly higher than when they left them in the morning. Troops of both species used >80 individual sites, the majority being used once. Mustached tamarins never used the same site for more than two consecutive nights, but saddlebacks reused the same site for up to four consecutive nights. Mustached tamarins slept at significantly greater heights than saddleback tamarins. There were consistent interspecific differences in the types of sites used. Neither the presence of infants, season, nor rainfall affected the types or heights of sites chosen. Sleeping sites were located in the central area of exclusive use more often than expected, and their position with respect to fruiting trees indicated a strategy closer to that of a multiple central place forager than a central place forager. These findings are discussed in light of species ecology, with particular reference to predation risk, which is indicated as the major factor influencing the pattern of sleeping site use in these species.

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.

Spatio‐genetic population structure in mustached tamarins, Saguinus mystax

Dispersal and philopatry influence gene flow and thus the spatio-genetic structure within and between populations. In callitrichids the flexible social and mating system corresponds with a variable migration pattern where both sexes might be philopatric or might disperse. We investigated the relationship between the spatio-genetic structure and migration patterns in a population of mustached tamarins, Saguinus mystax. Using the rapidly evolving hypervariable region I (HVI) of the mitochondrial control region and 11 microsatellite markers we detected a high variation (HVI: 16 haplotypes in 69 individuals; microsatellites: H(O) = 0.75, average: 7.45 alleles/locus), with mating partners usually not sharing the same haplotype, indicating that matings are generally between partners that are not closely related. Similar high variance of haplotype differences for male-male and female-female pairs, along with a slightly higher number of haplotype differences in males show that both sexes habitually migrate. Spatial analyses suggest that females usually migrate longer distances, corresponding to very limited breeding positions for females in a polyandrous social mating system.

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

AbstractStudies 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.

Dentition of moustached tamarins (Saguinus mystax mystax) from Padre Isla, Peru, part 1: Quantitative variation

Analyses of dental variation in geographically restricted, wild populations of primates are extremely rare; however, such data form the best source for models of likely degrees of variation within and between fossil species. Data from dental casts of a geographically restricted population of moustached tamarins (Saguinus mystax mystax) from Padre Isla, Peru, document high levels of dental variability, as measured by coefficients of variation, in a nonsexually dimorphic species, despite its isolation and small population size. Like other primates, moustached tamarins show lower variability in the dimensions of the first molars and increased variability in the dimensions of the final molars in the toothrow. Moustached tamarins from Padre Isla have a distinctive pattern of variability in the remaining teeth, including more stable tooth lengths in the anterior and posterior portions of the toothrow, and more stable tooth widths in the midregion of the toothrow. High variability in incisor width may be due to age effects of a distinctive diet and pattern of dental wear.