Saguinus Oedipus Research Articles

What is your diagnosis? Blood smear review from a cotton-top tamarin.

What is your diagnosis? Blood smear review from a cotton-top tamarin.

Factors influencing the survival of wild cotton-top tamarin (Saguinus oedipus) infants.

Studies of cooperative breeding species have suggested that helpers are needed for infant survival and that helpers gain skills to successfully raise their own offspring. Studies of callitrichids in managed care and early field studies suggested that group size correlated with infant survival and that helpers needed to learn parental skills to be successful breeders. We present infant survival data from a 20-year field study of cotton-top tamarins (Saguinus oedipus) in Colombia involving 126 litters born to 41 females. There was no difference in the survival of male and female offspring to 6 months of age. However, litter size impacted survival, with triplet litters having lower survival and male triplets having lower survival than females. Loss of infants was highest in the first week of life and, of the animals remaining in the group at 6 months of age, 90% of them survived to 1 year. The mean length of time in the natal group was 2.3 years but some young migrated to other groups after 4 months of age. Group size and number of male helpers (>1 year) was not related to infant survival. However, groups with only one male had fewer surviving infants. Primiparous females had lower infant survival, but previous infant care experience by mothers as helpers had no effect on survival. A major cause of infant loss was group disruption due to deaths/evictions/loss of the reproductively active animals, or immigration of pregnant females. Thus, factors that cause a change in the stability of the reproductively active animals can disrupt group cohesion. Capture of individuals for the illegal pet trade, as well as habitat fragmentation, may increase competition between groups for access to territories and breeding opportunities. This may have long-term impacts to infant survival in this critically endangered species.

Scent Marks Signal Species, Sex, and Reproductive Status in Tamarins (Saguinus spp., Neotropical Primates).

Olfactory communication is an important mediator of social interactions in mammals, thought to provide information about an individual’s identity and current social, reproductive, and health status. In comparison with other taxa such as carnivores and rodents, few studies have examined primate olfactory communication. Tamarins (Callitrichidae) conspicuously deposit odorous secretions, produced by specialized scent glands, in their environment. In this study, we combined behavioral and chemical data on captive cotton-top tamarins, Saguinus oedipus, and bearded emperor tamarins, S. imperator subgrisescens, to examine the role of olfactory communication in the advertisement of species, sex, and reproductive status. We observed no difference in scent-marking behavior between species; however, females marked more frequently than males, and reproductive individuals more than non-reproductive ones. In addition, tamarins predominantly used their anogenital gland when scent-marking, followed by the suprapubic gland. We collected swabs of naturally deposited tamarin anogenital scent marks, and analyzed these samples using headspace gas chromatography-mass spectrometry. Despite a limited sample size, we established differences in tamarin anogenital mark chemical composition between species, sex and reproductive status, and identified 41 compounds. The compounds identified, many of which have been reported in previous work on mammalian semiochemistry, form targets for future bioassay studies to identify semiochemicals. Our non-invasive method for collecting deposited scent marks makes it a promising method for the study of olfactory communication in scent-marking animal species, applicable to field settings and for the study of elusive animals.

Active sharing of a novel, arbitrary innovation in captive cotton-top tamarins?

Abstract Most cultural behaviours in primates stem from innovations that are beneficial since they provide access to food or comfort. Innovations that are seemingly purposeless and arbitrary, and nevertheless spread through a social group, are rarer but particularly relevant to understanding the evolutionary origin of culture. Here, we provide an anecdotal report of a series of non-instrumental woodchip manipulation and modification events in captive cotton-top tamarins. Intriguingly, woodchips were preferentially manipulated in a position that was readily visible to a partner in a different enclosure, and the innovation apparently spread to other individuals. Together, this suggests that the arbitrary innovation was actively shared with a conspecific, which is consistent with the pattern of transmission of another arbitrary innovation in cotton-top tamarins, namely stick-weaving.

P38γ Activation and BGP (Biliary Glycoprotein) Induction in Primates at Risk for Inflammatory Bowel Disease and Colorectal Cancer-A Comparative Study with Humans.

Colorectal cancer (CRC) is a common cause of cancer-related deaths largely due to CRC liver metastasis (CRLM). Identification of targetable mechanisms continues and includes investigations into the role of inflammatory pathways. Of interest, MAPK is aberrantly expressed in CRC patients, yet the activation status is not defined. The present study assessed p38γ activation in CRC patients, cancer cells, and tissues of cotton top tamarin (CTT) and common marmoset (CM). The primate world is an overlooked resource as colitis-CRC-prone CTT are usually inure to liver metastasis while CM develop colitis but not CRC. The results demonstrate that p38γ protein and phosphorylation levels are significantly increased in CRC patients compared to normal subjects and CTT. Furthermore, p38γ phosphorylation is significantly elevated in human CRC cells and hepatoblastoma cells but not in CM colon. Additionally, carcinoembryonic antigen (CEA) and biliary glycoprotein (BGP) are induced in the CRC patients that showed p38γ phosphorylation. Inhibition of p38 MAPK in CRC cells showed a significant decline in cell growth with no effect on apoptosis or BGP level. Overall, p38γ is activated in CRC tumorigenesis and likely involves CEA antigens during CRLM in humans but not in the CTT or CM, that rarely develop CRLM.

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).

Urogenital Lesions in Nonhuman Primates at 2 National Primate Research Centers.

Given their genetic and anatomic similarities to humans, nonhuman primates (NHPs) may serve as animal models for urogenital diseases of humans. The purpose of this study was to examine the frequency of spontaneous urogenital lesions occurring over a 30-year period at the Yerkes and Southwest National Primate Research Centers and to compare and contrast lesions occurring in Old World versus New World primates. Lesions occurring in the chimpanzee (Pan troglodytes), baboon (Papio spp.), rhesus macaque (Macaca mulatta), cynomolgus macaque (Macaca fascicularis), pig-tailed macaque (Macaca nemestrina), sooty mangabey (Cercocebus atys), common marmoset (Callithrix jacchus), cotton-top tamarin (Sanguinus oedipus), and squirrel monkey (Saimiri sciureus) are discussed. The most common lesions of the kidney were medullary amyloidosis, renal cysts, renal tubular degeneration, glomerulonephritis or glomerulopathy, nephritis, nephrocalcinosis, pyelonephritis, and hydronephrosis. Specific causes of renal tubular disease included pigmentary nephrosis and tubular lipidosis. Renal tumors, including renal adenoma and carcinoma, lymphoma, and nephroblastoma, were infrequent diagnoses in all species. Endometriosis was the most frequently diagnosed lesion of the female genital tract. Of the animals examined in this study, it was most frequent in Old World primates. Leiomyoma was the most common uterine tumor. Granulosa cell tumor was the most frequently observed neoplasm of the ovaries, followed by teratoma. Of animals included in the study, most ovarian tumors occurred in baboons. Neoplasms of the male reproductive tract included interstitial cell tumor, seminoma, penile squamous cell carcinoma, penile papilloma, and histiocytoma. In New World monkeys, renal lesions were reported more frequently than genital lesions.

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).

Jazz cats

Jazz cats

Draft Genome Sequences of Novel Campylobacter Species Isolated from Nonhuman Primates.

Campylobacter species are being increasingly isolated and associated with disease in humans and animals. Here, we describe four draft genome sequences of Campylobacter species from nonhuman primates. These include Campylobacter troglodytis, isolated from wild chimpanzees, and two likely new Campylobacter species isolated from a lemur, common marmoset, and cotton-top tamarin.

In Vivo Characterization of a Bank Vole-Derived Cowpox Virus Isolate in Natural Hosts and the Rat Model.

Cowpox virus (CPXV) belongs to the genus Orthopoxvirus in the Poxviridae family and is endemic in western Eurasia. Based on seroprevalence studies in different voles from continental Europe and UK, voles are suspected to be the major reservoir host. Recently, a CPXV was isolated from a bank vole (Myodes glareolus) in Germany that showed a high genetic similarity to another isolate originating from a Cotton-top tamarin (Saguinus oedipus). Here we characterize this first bank vole-derived CPXV isolate in comparison to the related tamarin-derived isolate. Both isolates grouped genetically within the provisionally called CPXV-like 3 clade. Previous phylogenetic analysis indicated that CPXV is polyphyletic and CPXV-like 3 clade represents probably a different species if categorized by the rules used for other orthopoxviruses. Experimental infection studies with bank voles, common voles (Microtus arvalis) and Wistar rats showed very clear differences. The bank vole isolate was avirulent in both common voles and Wistar rats with seroconversion seen only in the rats. In contrast, inoculated bank voles exhibited viral shedding and seroconversion for both tested CPXV isolates. In addition, bank voles infected with the tamarin-derived isolate experienced a marked weight loss. Our findings allow for the conclusion that CPXV isolates might differ in their replication capacity in different vole species and rats depending on their original host. Moreover, the results indicate host-specific differences concerning CPXV-specific virulence. Further experiments are needed to identify individual virulence and host factors involved in the susceptibility and outcome of CPXV-infections in the different reservoir hosts.

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.

Inferential reasoning in the visual and auditory modalities by cotton-top tamarins (Saguinus oedipus).

Nonhuman primate species appear to vary markedly in inferential reasoning abilities as measured by a classic inference-by-exclusion cup task. Even within species, individuals who can solve the cup task in the visual domain often struggle to use analogous auditory cues. Here we tested five cotton-top tamarins (Saguinus oedipus), cooperatively breeding New World monkeys that use both visual and auditory information when foraging, to investigate whether they might be able to solve the inference-by-exclusion task in both domains. Four subjects completed the testing series in both domains. Although three subjects performed well in the visual task, only one subject chose food location significantly above chance in response to positive auditory cues. These results demonstrate the first evidence of inferential reasoning abilities in a callitrichid species, while also revealing the performance asymmetry between the visual and auditory modalities observed in many other primates. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Systems Underlying Human and Old World Monkey Communication: One, Two, or Infinite.

Using artificially synthesized stimuli, previous research has shown that cotton-top tamarin monkeys easily learn simple AB grammar sequences, but not the more complex AnBn sequences that require hierarchical structure. Humans have no trouble learning AnBn combinations. A more recent study, using similar artificially created stimuli, showed that there is a neuroanatomical difference in the brain between these two kinds of arrays. While the simpler AB sequences recruit the frontal operculum, the AnBn array recruits the phylogenetically newer Broca’s area. We propose that on close inspection, reported vocal repertoires of Old World Monkeys show that these nonhuman primates are capable of calls that have two items in them, but never more than two. These are simple AB sequences, as predicted by previous research. In addition, we suggest the two-item call cannot be the result of a combinatorial operation that we see in human language, where the recursive operation of Merge allows for a potentially infinite array of structures. In our view, the two-item calls of nonhuman primates result from a dual-compartment frame into which each of the calls can fit without having to be combined by an operation such as Merge.

Positional encoding in cotton-top tamarins (Saguinus oedipus)

Strategies used in artificial grammar learning can shed light into the abilities of different species to extract regularities from the environment. In the A(X)nB rule, A and B items are linked, but assigned to different positional categories and separated by distractor items. Open questions are how widespread is the ability to extract positional regularities from A(X)nB patterns, which strategies are used to encode positional regularities and whether individuals exhibit preferences for absolute or relative position encoding. We used visual arrays to investigate whether cotton-top tamarins (Saguinusoedipus) can learn this rule and which strategies they use. After training on a subset of exemplars, two of the tested monkeys successfully generalized to novel combinations. These tamarins discriminated between categories of tokens with different properties (A, B, X) and detected a positional relationship between non-adjacent items even in the presence of novel distractors. The pattern of errors revealed that successful subjects used visual similarity with training stimuli to solve the task and that successful tamarins extracted the relative position of As and Bs rather than their absolute position, similarly to what has been observed in other species. Relative position encoding appears to be favoured in different tasks and taxa. Generalization, though, was incomplete, since we observed a failure with items that during training had always been presented in reinforced arrays, showing the limitations in grasping the underlying positional rule. These results suggest the use of local strategies in the extraction of positional rules in cotton-top tamarins.

Supplemental Material for Inferential Reasoning in the Visual and Auditory Modalities by Cotton-Top Tamarins (Saguinus oedipus)

Supplemental Material for Inferential Reasoning in the Visual and Auditory Modalities by Cotton-Top Tamarins (Saguinus oedipus)

Gamma-glutamyltranspeptidase expression by Helicobacter saguini, an enterohepatic Helicobacter species isolated from cotton top tamarins with chronic colitis.

Helicobacter saguini is a novel enterohepatic Helicobacter species isolated from captive cotton top tamarins with chronic colitis and colon cancer. Monoassociated H.saguini infection in gnotobiotic IL-10-/- mice causes typhlocolitis and dysplasia; however, the virulent mechanisms of this species are unknown. Gamma-glutamyltranspeptidase (GGT) is an enzymatic virulence factor expressed by pathogenic Helicobacter and Campylobacter species that inhibits host cellular proliferation and promotes inflammatory-mediated gastrointestinal pathology. The aim of this study was to determine if H.saguini expresses an enzymatically active GGT homologue with virulence properties. Two putative GGT paralogs (HSGGT1 and HSGGT2) identified in the H.saguini genome were bioinformatically analysed to predict enzymatic functionality and virulence potential. An isogenic knockout mutant strain and purified recombinant protein of HSGGT1 were created to study enzymatic activity and virulence properties by in vitro biochemical and cell culture experiments. Bioinformatic analysis predicted that HSGGT1 has enzymatic functionality and is most similar to the virulent homologue expressed by Helicobacter bilis, whereas HSGGT2 contains putatively inactivating mutations. An isogenic knockout mutant strain and recombinant HSGGT1 protein were successfully created and demonstrated that H.saguini has GGT enzymatic activity. Recombinant HSGGT1 protein and sonicate from wild-type but not mutant H.saguini inhibited gastrointestinal epithelial and lymphocyte cell proliferation without evidence of cell death. The antiproliferative effect by H.saguini sonicate or recombinant HSGGT1 protein could be significantly prevented with glutamine supplementation or the GGT-selective inhibitor acivicin. Recombinant HSGGT1 protein also induced proinflammatory gene expression in colon epithelial cells. This study shows that H.saguini may express GGT as a potential virulence factor and supports further in vitro and in vitro studies into how GGT expression by enterohepatic Helicobacter species influences the pathogenesis of gastrointestinal inflammatory diseases.

How long does it take? Reliable personality assessment based on common behaviour in cotton-top tamarins (Saguinus oedipus)

Individual variation in behaviour has been shown to have important ecological and evolutionary consequences. Research on animal personality has therefore received considerable attention, yet some methodological issues remain unresolved. We tested whether assessing personality by coding common behaviours is as time-consuming method as some researchers believe it to be. Altogether, 300 hours of observation were collected on 20 captive cotton-top tamarins (Saguinus oedipus). We first examined the repeatability of behavioural indices that represented the behavioural repertoire of cotton-top tamarins. We then compared the personality structures, based on different lengths of observation time, of these behavioural indices. The minimum observational time necessary to obtain a stable personality structure was 5 to 7 hours per individual. This stable structure included two components: Extraversion and Confidence, which were similar to those described in great apes, Old World monkeys, and other New World monkeys. Our findings suggest that, at least in the case of cotton-top tamarins, behavioural coding over relatively short periods of time can be used to assess personality and that longer observation periods may yield diminishing returns.

Bifidobacterium primatium sp. nov., Bifidobacterium scaligerum sp. nov., Bifidobacterium felsineum sp. nov. and Bifidobacterium simiarum sp. nov.: Four novel taxa isolated from the faeces of the cotton top tamarin (Saguinus oedipus) and the emperor tamarin (Saguinus imperator)

Four novel Gram-stain-positive, non spore forming and fructose-6-phosphate phosphoketolase-positive strains were isolated from the faeces of a cotton top tamarin (Saguinus oedipus) and an emperor tamarin (Saguinus imperator). Phylogenetic analyses based on 16S rRNA revealed that bifidobacterial strains TRE 1T exhibit close phylogenetic relatedness to Bifidobacterium catulorum DSM 103154 (96.0%) and Bifidobacterium tissieri DSM 100201 (96.0%); TRE DT and TRE HT were closely related to Bifidobacterium longum subsp. longum ATCC 15708T with similarity values of 97.4% and 97.5%, respectively; TRI 7T was closely related to Bifidobacterium tissieri DSM 100201 (96.0%). The Average Nucleotide Identity (ANI) and in silico DDH (isDDH) analysis with closest neighbour supported an independent phylogenetic position of all strains with values ranged from 74 to 85% for ANI and from 24 to 28% for isDDH. DNA base composition of the four strains was in the range of 58.3–63.5mol% G+C. Based on the phylogenetic, genotypic and phenotypic data, the strains TRE 1T, TRE DT, TRE HT and TRI 7T clearly represent four novel taxa within the genus Bifidobacterium for which the names Bifidobacterium primatium sp. nov. (type strain TRE 1T=DSM 100687T=JCM 30945T), Bifidobacterium scaligerum sp. nov. (type strain TRE DT=DSM 103140T=JCM 31792T), Bifidobacterium felsineum sp. nov. (type strain TRE HT=DSM 103139T=JCM 31789T) and Bifidobacterium simiarum sp. nov. (type strain TRI 7T=DSM 103153T=JCM 31793) are proposed.

Phenotypic, Genetic, and Cytogenetic Evidence of Hybridization Between Species of Trans-Andean Tamarins (Genus Saguinus)

Incomplete reproductive isolation and hybridization is relatively frequent in primates. However, no cases of hybridization between formally recognized species have been reported in tamarins (genus Saguinus), a highly specious group of Neotropical primates. Here, we provide evidence from different sources to demonstrate three cases of hybridization in captivity between species of Saguinus distributed west of the Andes (trans-Andean). To do this, we described fur color patterns, genotyped 12 microsatellite loci, sequenced the mitochondrial hypervariable region I, and generated chromosomal R bands for the three formally recognized species and the new hybrids of trans-Andean tamarins. We identified one case of interbreeding between the white-footed tamarin (Saguinus leucopus) and the cotton-top tamarin (S. œdipus) and two independent reciprocal crosses of S. leucopus and the Geoffroy’s tamarin (S. geoffroyi). All these hybrids exhibit intermediate phenotypes between parental species, and genetic data are consistent with first-generation hybridization. Cytogenetic data suggest that the S. leucopus × S. œdipus hybrid is sterile, as it is a female with XY karyotype apparently affected by a condition known as gonadal dysgenesis. Trans-Andean tamarin species occur in northwest Colombia with parapatric distributions bounded by major rivers. Potential contact zones, either natural or anthropogenic, might facilitate hybridization in the wild, but this scenario remains to be assessed. Our findings warrant future studies focused on the evolutionary mechanisms of reproductive isolation in tamarins. Given the risk of hybridization, caution should be taken in management and conservation of tamarins.