Saguinus Midas Research Articles

A new species of Demodex (Acari: Demodecidae) from the skin of golden-handed tamarins, Saguinus midas (Primates: Cebidae)

Two captive-bred golden-handed tamarins, Saguinus midas L., 1758 (Primates: Cebidae), kept in households in Japan, presented with psoriasis-like plaques on their faces, along with scale, alopecia, and itching. Histopathological examination revealed numerous Demodex mites in the hair follicles, and the clinical symptoms in both cases improved after treatment with fluralaner. Based on the morphological and genetic characteristics of the mites collected from tamarins, we describe a new species of Demodex. This new species is the fifth valid Demodex species recorded from primates.

Keeping primates as pets in the Czech Republic

Primates belong to the most endangered groups of animals on Earth and their keeping in captivity is usually associated with the need to protect endangered species and create a viable reserve population. However, primates are also kept as pets. The aim of the study was to assess the species and numbers of primates kept in the Czech Republic as pets; for comparison, the species and numbers of primates kept in Czech zoos were also monitored. According to the CITES register, a total of 7,708 primates of 79 species from nine families were kept in both types of facilities (data valid as of 31 December 2020). Of these, 3,821 individuals were kept as pets and 3,877 in zoos. The most commonly kept species were the western pygmy marmoset, common marmoset, golden-handed tamarin, Guianan squirrel monkey from the Cebidae family, ring-tailed lemurs and black-and-white ruffed lemur from the Lemuridae family, mandrill, guereza, Japanese macaque, and bonnet macaque from the Cercopithecidae family. No primates of the Hominidae and Atelidae families were recorded in the case of pet keeping. The results show that in the Czech Republic, the number of primates kept as pets is comparable to their numbers in zoos. However, the question is whether this is a positive finding, given the difficulty of creating conditions for pet primates that meet their requirements, and also given that the contribution of pet keeping to the preservation of their population on Earth is questionable.

Birds of a feather speak together: Understanding the different dialects of animals can help to decipher their communication.

As humans, many animal species that communicate via vocalization show a wide range of accents and dialects driven by environmental and social factors.

Convergent character displacement in sympatric tamarin calls (Saguinus spp.)

Character displacement, or a shift in traits where species co-occur, is one of the most common ecological patterns to result from interactions between closely related species. Usually, character displacement is associated to divergence in traits, though, they might be convergent, especially when used for aggressive interference between species. In the context of animal communication, territorial calls are predicted to converge in order to increase context recognition and decrease the costs of ecological interference competition. However, such signals might also be adapted to characteristics of the shared environment. In this study, we used data from 15 groups of two parapatric tamarins, Saguinus midas and S. bicolor, to test for similarities in long calls among sympatric and allopatric groups. We hypothesized that calls would converge in sympatric areas, as it would be mutually beneficial if both species recognize territorial contexts, but that convergence would depend on forest type due to acoustic adaptation. As predicted, long calls converged in sympatry, with S. midas shifting its calls towards S. bicolor’s acoustic pattern. However, this shift only occurred in primary forest. In sympatric areas, S. midas produced sounds with narrower bandwidths in primary than in secondary forest, consistent with optimization of sound propagation while both species produced longer calls in primary forests independently of geographic location (i.e. sympatry and allopatry). Our results suggest that both social and environmental pressures are important in shaping tamarin sounds. As their effects can interact, analyses, which assume that these ecological pressures act independently, are likely to miss important patterns. Territorial signals between closely related sympatric species are expected to be convergent to increase context recognition and decrease the costs of interference competition. However, such signals might also be adapted to characteristics of the shared environment, such as forest structure characteristics. We analysed vocalisations from two parapatric tamarins and found that, though their long calls asymmetrically converged in sympatry, only red-handed tamarins shifted towards pied tamarin call type, and this only occurred in primary forest. Our results suggest that both social and environmental pressures are important in shaping primate calls. Because their effects can interact, analyses which assume that these pressures act independently, are likely to miss important patterns.

Parapatric pied and red-handed tamarin responses to congeneric and conspecific calls

Aggressive behaviors are widespread among territorial species and asymmetrical aggressiveness may imply differential access to resources. At a larger scale, such asymmetry may also drive shifts in geographic distributions. The pied tamarin (Saguinus bicolor) is an endangered Amazonian primate species with a small natural range. In recent decades further reduction of its range has been observed coincident with the expansion of the range of the red-handed tamarin's (Saguinus midas), which appears to be encroaching into the area otherwise occupied by the pied tamarin. Here we test if, at range boundaries, red-handed tamarin produces more aggressive vocalizations than the pied tamarin. We performed a series of 96 playback trials presenting both congeneric and conspecific long calls to sixteen groups of red-handed tamarins and fourteen of pied tamarins. We recorded their territorial, agonistic, alarm vocalizations, and the duration of their calling displays after broadcasts. In doing so, we assessed whether agonistic displays were more likely to occur in response to congeneric than conspecific calls in areas of sympatry. We found that the red-handed tamarin was more likely to emit more territorial calls when listening to pied tamarins than to its own species in sympatric areas, but found no differences in vocal responses from either species in relation to agonistic calls or duration of display in sympatric and allopatric areas. Furthermore, the red-handed tamarin emitted more alarm calls when listening to pied tamarin, independently of the geographic circumstances. Overall, we found that acoustic displays may be mediating species interaction in areas of sympatry. Together, these observations are suggestive of behavioral interference, including the competitive displacement of pied tamarin by red-handed tamarins.

Comparative assessment of behaviorally derived personality structures in golden-handed tamarins (Saguinus midas), cotton-top tamarins (Saguinus oedipus), and common marmosets (Callithrix jacchus).

One way to address questions about the origins and adaptive significance of personality dimensions is by comparing the personality structures of closely related species that differ in their socioecological circumstances. For the present study, we compared the personalities of captive golden-handed tamarins (Saguinus midas; N = 28), cotton-top tamarins (Saguinus oedipus; N = 20), and common marmosets (Callithrix jacchus; N = 17). All 3 species are New World monkeys of the family Callitrichidae. They thus share reproductive and behavioral characteristics but differ some in terms of their diet, habitat, and social organization. We expected that personality structures of closely related tamarin species would overlap more, both in terms of number of dimensions and their content, than either would overlap with the personality structure of common marmosets. We assessed personality using behavioral observations and compared the personality structures by means of cross-species correlations and fuzzy set analyses. Principal component analyses identified components that we labeled Agreeableness, Assertiveness, and Extraversion in golden-handed tamarins and common marmosets and components labeled Confidence and Extraversion in cotton-top tamarins. The greater personality similarities of the two phylogenetically more distant species suggest that differences in social organization, and in both habitat diversity and complexity, contributed to the evolution of personality. However, we also found that behaviors clustered in similar ways in the two tamarin species, suggesting that phylogenetic relatedness and genus-specific socioecological characteristics, such as the degree of reproductive competition, shaped personality structure in this primate family. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Gum feeder as environmental enrichment for zoo marmosets and tamarins.

Tamarins and marmosets are small-bodied social callitrichines. Wild callitrichines feed on exudates, such as sap and gum; particularly, marmosets are mainly gummivores, while tamarins consume gums only occasionally and opportunistically. Zoo marmosets and tamarins are usually provided with gum arabic as an alternative to the exudates normally found in the wild. The aim of this study was to evaluate the effects of a gum feeder on the behavior and well-being of four zoo-managed callitrichines. We studied four cotton-top tamarins (Saguinus oedipus), four red-handed tamarins (S. midas), two pygmy marmosets (Cebuella pygmaea), and three Geoffroy's marmosets (Callithrix geoffroyi) housed at Parco Natura Viva (Italy). We conducted the study over two different periods, a baseline (control, without the gum feeder) and then a gum feeder (when the gum feeder was provided) period. We used continuous focal animal sampling to collect behavioral data, including durations of social and individual behaviors. We collected 240 min of observations per period per study subject, with a total of 3,120 min for all the subjects in the same period and of 6,240 min in both periods. We analyzed data by using nonparametric statistical tests. First, we found that the gum feeder promoted species-specific behaviors, such as exploration, and diminished self-directed behaviors, suggesting an enriching effect on tamarin and marmoset behavior. Moreover, in red-handed tamarins, the provision of the gum feeder reduced the performance of self-directed and abnormal behavior, specifically coprophagy. These results confirm that gum feeders are effective foraging enrichment tools for zoo marmosets and tamarins.

SUCCESSFUL TREATMENT OF GENERALIZED DEMODICOSIS IN RED-HANDED TAMARINS ( SAGUINUS MIDAS) USING A SINGLE ADMINISTRATION OF ORAL FLURALANER.

Two adult sibling red-handed tamarins ( Saguinus midas) presented with weight loss and multifocal skin masses. A skin biopsy revealed pyogranulomatous dermatitis with intrafollicular Demodex sp. mites. Subsequent skin scrapes confirmed the presence of live mites within lesions. Initial treatment with topical and oral ivermectin was unsuccessful, and lesions continued to progress. A single dose of fluralaner (Bravecto®, Merck Animal Health, Kenilworth, New Jersey, 07033, USA; 28.125 mg po) was administered to each animal approximately 5 mo after initial presentation. Lesions resolved over the next 3 mo, and all follow-up skin scrapes were negative for both animals. No adverse effects were noted. A single oral administration of fluralaner at 30-35 mg/kg appears adequate and safe for the treatment of generalized demodicosis in red-handed tamarins.

Behavior of tamarins, tanagers and manakins foraging in a strangler fig (Ficus sp.) in Suriname, South America: implications for seed dispersal

The behavior of foragers can directly affect the dispersal of seeds. Strangler figs are keystone resources throughout the tropics and are important resources for both primates and birds. We examined the foraging behavior of golden-handed tamarins and four bird species in a strangler fig to see how these behaviors might affect the dispersal of fig seeds. Tamarins removed fruit at a faster rate than did any of the bird species examined. Additionally, tamarins tended to swallow figs whole whereas birds tended to drop figs once they were processed. Tamarins visiting fig trees ingest large quantities of fig seeds that may be deposited throughout the forest. Birds on the other hand tended to slowly process fruits near the fig tree and drop processed fruit containing large quantities of seeds. Future studies need to be conducted to ascertain differences in post dispersal seed fate.

Prevalence and Molecular Phylogenetic Characterization of Trypanosoma (Megatrypanum) Minasense in the Peripheral Blood of Small Neotropical Primates After a Quarantine Period

Neotropical primates of the Cebidae and Callitrichidae, in their natural habitats, are frequently infected with a variety of trypanosomes including Trypanosoma cruzi, which causes a serious zoonosis, Chagas' disease. The state of trypanosome infection after a 30-day quarantine period was assessed in 85 squirrel monkeys (Saimiri sciureus) and 15 red-handed tamarins (Saguinus midas), that were wild-caught and exported to Japan as companion animals or laboratory animals, for biomedical research, respectively. In addition to many microfilariae of Mansonella (Tetrapetalonema) mariae at a prevalence of 25.9%, and Dipetalonema caudispina at a prevalence of 3.5%, a few trypomastigotes of Trypanosoma (Megatrypanum) minasense were detected in Giemsa-stained thin films of blood from 20 squirrel monkeys at a prevalence of 23.5%. Although few T. minasense trypomastigotes were found in Giemsa-stained blood films from tamarins, a buffy-coat examination detected trypanosomes in 12 red-handed tamarins (80.0%), and PCR amplification of a highly variable region of the small subunit ribosomal RNA genes (SSU rDNA) for Trypanosoma spp. detected the infection in 14 of the 15 tamarins (93.3%). Nucleotide sequences of the amplicons were identical for trypanosomes from tamarins and squirrel monkeys, indicating a high prevalence but low parasitemia of T. minasense in imported Neotropical nonhuman primates. Based on the SSU rDNA and 5.8S rDNA, the molecular phylogenetic characterization of T. minasense indicated that T. minasense is closely related to trypanosomes with Trypanosoma theileri-like morphology and is distinct from Trypanosoma (Tejeraia) rangeli, as well as from T. cruzi. Using some blood samples from these monkeys, amplification and subsequent sequencing of the glycosomal glyceraldehyde-3-phosphate dehydrogenase (gGAPDH) gene fragments detected 4 trypanosome genotypes, including 2 types of T. cruzi clade, 1 type of T. rangeli clade, and 1 T. rangeli-related type, but failed to indicate its phylogenetic position based on the gGAPDH gene. Furthermore, species ordinarily classified in the Megatrypanum by morphological criteria do not form a clade in any molecular phylogenetic trees based on rDNA or gGAPDH genes.

A Survey of Primate Populations in Northeastern Venezuelan Guayana

The region of the Guiana Shield is extraordinarily rich in biodiversity. Little is known, however, of the biogeography and conservation status of its diverse primate taxa. The aim of this study was to conduct a rapid survey of primate populations in the northeastern-most part of the state of Bolívar, Venezuela, near the border with Guyana. A previous study had indicated that the white-faced saki (Pithecia pithecia), wedge-capped capuchin (Cebus olivaceus), and red howler monkey (Alouatta seniculus) were present in this area. It had also been suggested that black spider monkeys (Ateles paniscus), golden-handed tamarins (Saguinus midas), and night monkeys (Aotus) may be present in this part of the Venezuelan Guayana. Forty-nine sites of the Río Cuyuní basin were surveyed. Pre-existing forest trails were walked and the Río Cuyuní was also censused by boat. Interviews with local people at all the sites indicated that the only primates inhabiting this region are A. seniculus, C. olivaceus, and P. pithecia. S. midas is not present (or is extremely rare) in the northeastern part of the state of Bolívar. References to night monkeys may well refer to Potos flavus. The presence of an isolated population of Ateles remains uncertain. Cattle ranching, mining, hunting, logging, and the pet trade are major threats to the primates in this part of Venezuela. Further primate surveys should be conducted in the western Guiana Shield.

Biogeography of the Primates of Guyana: Effects of Habitat Use and Diet on Geographic Distribution

Species that exploit a wide range of resources or habitats (generalists) tend to be widely distributed, whereas species that exploit a narrow range of resources or habitats (specialists) often have a limited distribution. The distribution patterns are thought to result from specialists using relatively smaller habitats than those exploited by generalists. I used data from 1,725 km of primate surveys that I conducted in Guyana to test these hypotheses. Habitat breadth is the total number of different habitat types occupied by each species. I used the total number of different food categories exploited by each species to measure dietary breadth. Geographic range size is correlated with habitat breadth but not with dietary breadth or body size for the 8 primate species in Guyana. Habitat generalists—red howlers and wedge-capped capuchins—range into all habitats. Habitat specialists—spider monkeys, brown bearded sakis, and golden-handed tamarins—range only into large habitats. Habitat generalists tend to be dietary type specialists in Guyana. I suggest that only habitat generalists can subsist on the low-quality foods in small habitats in Guyana. Conversely, habitat specialists tend to be dietary type generalists in Guyana. They must feed on a variety of food types in large habitats. However, using the number of food categories exploited as a measure of dietary breadth may be only a weak aspect of multidimensional niche. Researchers testing biogeographic hypotheses associated with dietary breadth should consider including multivariate indicators of both the types of food categories eaten and the number of plant species exploited.

Novel gamma-1 herpesviruses identified in free-ranging new world monkeys (golden-handed tamarin [Saguinus midas], squirrel monkey [Saimiri sciureus], and white-faced saki [Pithecia pithecia]) in French Guiana.

The recent finding of a novel Epstein-Barr virus-related lymphocryptovirus (CalHV-3) in a captive colony of common marmoset (Callithrix jacchus) in the United States modifies the view that the host range of lymphocryptovirus is restricted to humans and Old World primates. We investigated the presence of Epstein-Barr virus-related viruses in 79 samples of New World monkeys caught in the wild, including six species of the Cebidae family and one of the Callitrichidae, living in the rain forest of French Guiana. Using a degenerate consensus PCR method for the herpesvirus DNA polymerase gene, we identified three novel lymphocryptoviruses from golden-handed tamarin (Saguinus midas) of the Callitrichidae family and squirrel monkey (Saimiri sciureus) and white-faced saki (Pithecia pithecia) of the Cebidae family. With the CalHV-3 strain, these three novel viruses constitute a well-supported phylogenetic clade in the Lymphocryptovirus genus, which is clearly distinct from the lineage of Old World lymphocryptovirus, hosted by catarrhine monkeys and humans. In tamarins, the prevalence of the novel lymphocryptovirus was more than 50%, indicating that it circulates well in the wild population, perhaps due to specific ecoethological patterns such as confrontations and intergroup migration. The detection and partial molecular characterization of the polymerase gene of three novel Gamma-1-Herpesvirinae from New World monkeys caught in the wild clearly indicate that free-ranging populations of platyrrhine are natural hosts of lymphocryptoviruses. Further characterization of these novel viruses will provide new insight not only into the origin and evolution of Gammaherpesvirinae but also into their pathogenicity.

Health evaluation of translocated free-ranging primates in French Guiana.

Among over 40 mammal species threatened by the filling of a hydroelectric dam reservoir in French Guiana, three species of primates have been translocated, comprising 124 red howler monkeys, six white-faced sakis, and 95 golden-handed tamarins. Health status of the animals was evaluated by direct physical examination and by hematological, biochemical, virological, and parasitological surveys of collected blood. The physical condition of the howlers was slightly worse toward the end of the capture period, but that of sakis and tamarins remained satisfactory. Several ectoparasites (ticks, larvae of dipterous insects, fleas, and lice) were collected, and various wounds, apparently nondebilitating, were recorded in howlers. Hematological and biochemical profiles determined for the three species revealed a slight anemia in howlers. Entamoeba, Strongyloides, and Trypanoxyurus were common in fecal samples of howlers. A survey of blood smears from the three species revealed infection by several types of microfilaria, Trypanosoma rangeli-like and Plasmodium brasilianum in all three, and Trypanosoma cruzi-like in howlers. These infections had no significant impact on the health status or the hematological profiles. Serologic investigations revealed occasional reactions against Toxoplasma gondii, a strong anti-Plasmodium response in the two Cebidae species, and a weaker one in tamarins. Attempts to isolate arbovirus failed, but antibody responses to Mayaro and yellow fever viruses were strong, especially in the howlers. A strong correlation between age and serological status led to a better understanding of the epidemic cycles. Our survey indicates French Guianan primates are reservoirs for several anthropozoonoses, including malaria, Chagas disease, and arboviruses.

Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates

This study examines behavioral affective reactions elicited by tastes from eight newborn human infants, and from 27 other infant or adult primates. Non-human primates belonged to 11 species: three great apes (chimpanzee, orangutan, gorilla), three Old World monkeys (rhesus monkey, greater spot-nosed monkey, and red-capped mangabey), four New World monkeys (golden-handed tamarin, cotton-top tamarin, white tufted-ear marmoset, and Humboldt's night monkey), and one lemur (mongoose lemur). The taste of sucrose elicited homologous positive hedonic patterns of facial affective reactions from humans and other primates, whereas quinine elicited homologous aversive or negative affective patterns. The degree of similarity between human and other primate affective reaction patterns appeared to be strongly indicative of their phylogenetic relatedness. For example, affective reaction patterns of human infants and great apes were more similar to each other than either were to Old World monkeys or New World monkeys. Certain affective reaction components were found to be shared by humans and all primates, whereas other components were restricted to particular taxonomic groups. Finally, allometric timing parameters for the duration of components indicated that the ‘same’ affective reaction could have different durations in species of different size. These results show that both positive/negative valence and intensity of affective reaction may be quantitatively assessed in human and non-human primates, and indicate that taste-elicited affective reaction patterns of human infants are related systematically to those of other primate species.

Conservation of Absolute Foveal Area in New World Monkeys

The foveal specializations of five New World monkeys, the marmoset, Callithrix jacchus; the golden-handed tamarin, Saguinus midas niger; the squirrel monkey, Saimiri ustius; the capuchin monkey, Cebus apella; and the howler monkey, Alouatta caraya were compared. Although retinal area varies by over a factor of two in these monkeys, the area of the fovea does not covary with retinal area and remains approximately the same absolute size, as measured by the dimensions of the high density region of cones, or the rod-free region. This constancy in foveal size also holds for rhesus monkeys and humans, bringing the variation in retinal area to a factor of five. Alouatta caraya is unusual, distinguished by a very high central cone density and a small rod-free zone. Physiological constraints that might limit foveal area over a wide range of eye sizes are considered.

Sleeping Site Selection by the Golden-handed Tamarin Saguinus midas midas: The Role of Predation Risk, Proximity to Feeding Sites, and Territorial Defence

Tamarin monkeys, of the genus Saguinus, spend over half their lives at arboreal sleeping sites. The decision as to which site to use is likely to have considerable fitness consequences. These decisions about sleeping sites by three troops of golden-handed tamarin Saguinus midas midas were examined over a 9-mo period at a rainforest site in French Guiana. Data are presented on the physical nature of sleeping sites, their number, position within home ranges, and pattern of use and reuse, aspects of behaviour at retirement and egress, and predation attempts on the study troops. Cumulative plot analysis indicated that a tamarin troop used 30-40 sleeping sites in a 100-day period, approximately half of which were used very infrequently, so that consecutive reuse was never greater than three nights. Sleeping trees were superior in architectural parameters and liana weight to non-sleeping trees. There were no more sleeping sites than expected within the home range boundary region of the tamarins or in areas of overlap with the home ranges of neighbouring troops. Tamarins selected sleeping sites nearest to the last feeding site of the day on 25% of occasions. The study troops engaged in a number of activities that may reduce predation risk; raptor attacks on the study troops over 9 mo were frequent but unsuccessful. Tamarins often visited a sleeping site several hours before arrival, and were more likely to visit a site before use if they had not used it recently. The decision to select a sleeping site therefore involved knowledge of the previous frequency of use of that site.

Primate species richness in relation to habitat structure in Amazonian rainforest fragments

Factors affecting species richness in fragmented habitat are often of interest to conservation programs. Groups of red howler monkeys Alouatta seniculus, white-faced sakis Pithecia pithecia and golden-handed tamarins Saguinus midas occurred in five small (approx. 10 ha) fragments of Amazonian rainforest. However, not all of these species occurred in every fragment. The purpose of this study was to identify some of the factors affecting the number and distribution of primate species among these areas. To determine whether habitat structural diversity influenced primate species richness, height, diameter at breast height (DBH) and number of trees, DBH and number of lianas (woody vines) as well as height and number of palms in 15 20 × 20 m quadrats in each fragment were recorded. Also, height and number of secondary growth plants surrounding reserves were sampled. Structurally ‘complex’ reserves had high mean number of trees, high mean number of lianas, low mean percentage large trees (> 10 cm DBH) per quadrat, and streams. These characteristics were correlated with high species richness. P. pithecia occurred in the most structurally ‘complex’ fragments, S. midas in fragments surrounded by relatively tall secondary growth and A. seniculus in all five fragments. The relationships between the habitat requirements of the three species and their occurrence in these fragments are discussed.