A tale of two hierarchies: Hormonal and behavioral factors underlying sex differences in social dominance in cooperative breeding callitrichids.

Callitrichid primates are recognized for high levels of sociality in small groups, their great behavioral flexibility, and single-female dominant hierarchies. Previous work has highlighted that dominant, breeding callitrichids engage in behavioral and hormonal reproductive suppression of related and unrelated subordinates by both producing more offspring, having higher levels of ovulatory hormones, and accessing more sociosexual opportunities. This suppression constitutes a nexus of changes in pituitary responsiveness, ovarian cyclicity, sexual behavior, affiliation, and aggression. In this review, I will highlight important features that characterize callitrichid social hierarchies across broad social contexts. Dominant females sometimes exert reproductive suppression on subordinate nonbreeding females, but this suppression varies across callitrichids based on social stability and changes in group composition, particularly related to the number, experience, and age of nonbreeding subordinates. Meanwhile, dominant males may induce suppression of reproduction in subordinate males, but these effects occur by different behavioral and endocrine mechanisms and to a much lesser extent than their female counterparts; While dominant female callitrichids usually show higher levels of aggression relative to their male counterparts, callitrichids show a general absence of intersexual dominance, likely as an effort of maintaining a cohesive breeding pair within a stable social group and social cooperation. Future efforts are needed to identify precise neuroendocrine mechanisms underlying the presence of sex differences in callitrichid behavior separate from peripheral reproductive function. This is especially important with regard to parental experience, social relationships, development and aging, with larger implications toward understanding sex differences in overall health and wellbeing.

Evaluating genital skin color as a putative sexual signal in wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins.

Coevolution between signalers and receivers has played a significant role in the diversity of animal signals and sensory systems. Platyrrhines (monkeys in the Americas) exhibit a remarkable color vision polymorphism that may have been selected by both natural and sexual selection, but sociosexual color signaling among platyrrhines has received almost no attention. Here, we study the color of reproductive skin among different reproductive classes in free-ranging female saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins, modeling color spaces, and contrasts for the different visual systems. We find that the chromatic saturation and luminance of genital color vary between reproductive classes in saddleback tamarins. Chromatic contrast between the vulva and belly is lower in the parous females (PFs) relative to adult but not currently breeding females, while achromatic contrast is higher in PFs in saddleback tamarins relative to nonparous females. However, in emperor tamarins, genital color (saturation, hue, and luminance) does not vary between reproductive classes. Overall, genital skin color variation is present in tamarins and may play a role in sexual signaling. Nevertheless, the patterns are inconsistent between species, suggesting interspecific variation. Future studies should integrate the perceiver's behavioral responses and the physical and social signaling environments into comprehensive studies of communication as well as consider the role and interaction between multiple sensory modalities.

A comparison of rectal and oral cultivable microbiota in wild and captive black lion tamarins (Leontopithecus chrysopygus, Mikan 1823).

The black lion tamarin (Leontopithecus chrysopygus) is an endangered primate species, restricted to the Atlantic Forest fragments of São Paulo state, Brazil, with an estimated wild population of ~1600 individuals. Integrative studies between zoo (ex situ) and wild (in situ) animals are crucial to modern conservation programs. They can demonstrate a substantial impact with the One Health concept, an interdisciplinary research frontier regarding the relations between human, animal, and environmental health. Studies of wild populations of Leontopithecus spp. are scarce and should be encouraged to provide baseline information to develop preventive and curative medicine in zoos and other conservation programs. Studying these animals in the wild can offer important reference parameters for the species. Comparing bacterial communities between in situ and ex situ populations can help us understand both conditions and the dynamics of potentially pathogenic microorganisms. To increase our understanding of resident microorganisms among these groups, we collected oral and rectal samples from captive (zoo) and wild black lion tamarins. We employed a culture method for the identification of aerobic bacteria. Thirty-three specimens were sampled (24 zoo and 8 wild animals) and 18 bacterial genera were identified. We found primarily Gram-positive bacteria in wild animals, whereas in zoo animals, Gram-negative bacteria were dominant. Some of the bacterial species we identified are potentially pathogenic, whereas several others are being reported here for the first time in this host species. Our results reinforce the importance of integrative studies for the future management and conservation of this endangered primate species.

Epidemiological, clinical and pathological aspects of lethal acanthocephalosis in captive neotropical primates.

BACKGROUND: Acanthocephalosis is an important cause of death in captive New World primates (NWP). Once established in a colony, it is extremely difficult to treat and control, quickly spreading among NWP with a high mortality rate. This study aimed to characterize the disease associated with infection with acanthocephalans according to its epidemiological, clinical, and anatomopathological aspects in a captive NWP population. METHODS: From 2010 to 2020, a Brazilian zoo had recurrent deaths of NWP associated to acanthocephalan parasitism. Clinical and pathological profiles of these animals were analyzed considering the host species, sex, age, weight, clinical signs, therapeutic protocols, and pathological findings. RESULTS: A total of 27 deaths associated with acanthocephalosis were recorded, all lethal cases affected tamarins and lion tamarins, corresponding to 67.5% of total deaths during the course of this study. Ten animals died with no previously detected clinical signs, whereas cases with noticeable clinical signs often had apathy and progressive weight loss, resulting in cachexia. Symptomatic NWP were treated with anthelmintic protocols, antibiotics, and support therapy. However, all hospitalized animals died and had grossly detectable adult acanthocephalans in the intestinal lumen that were identified as Prosthenorchis sp., which were associated with transmural and ulcerative enteritis. CONCLUSIONS: This report revealed the impact of acanthocephalosis in a naturally infected captive colony of NWP, particularly affecting tamarins (Saguinus spp.) and lion tamarins (Leontopithecus spp.), with failed treatment and control strategies.

Repetitive Sequence Distribution on Saguinus, Leontocebus and Leontopithecus Tamarins (Platyrrhine, Primates) by Mapping Telomeric (TTAGGG) Motifs and rDNA Loci.

Tamarins are a distinct group of small sized New World monkeys with complex phylogenetic relationships and poorly studied cytogenetic traits. In this study, we applied molecular cytogenetic analyses by fluorescence in situ hybridization with probes specific for telomeric sequences and ribosomal DNA loci after DAPI/CMA3 staining on metaphases from five tamarin species, namely Leontocebus fuscicollis, Leontopithecus rosalia, Saguinus geoffroyi, Saguinus mystax and Saguinus oedipus, with the aim to investigate the distribution of repetitive sequences and their possible role in genome evolution. Our analyses revealed that all five examined species show similar karyotypes, 2n = 46, which differ mainly in the morphology of chromosome pairs 16-17 and 19-22, due to the diverse distribution of rDNA loci, the amplification of telomeric-like sequences, the presence of heterochromatic blocks and/or putative chromosomal rearrangements, such as inversions. The differences in cytogenetic traits between species of tamarins are discussed in a comparative phylogenetic framework, and in addition to data from previous studies, we underline synapomorphies and apomorphisms that appeared during the diversification of this group of New World monkeys.

On the way to systematize habituation: a protocol to minimize the effects of observer presence on wild groups of Leontocebus lagonotus.

Habituation is used in most field research with primates to minimize observer effects on their behavior. Despite its importance, there is little published on the methods used to habituate different taxa of primates or how these methods vary in different habitat types. We assessed changes in behavior and space use of two groups of Leontocebus lagonotus in the Ecuadorian Amazon in order to document this process. Although the subjects had not been studied before, visitors and researchers were more frequently in the home range of Group 1 than of Group 2. We followed both groups for 2 months, collecting behavioral data through scan sampling and recording the use of space (ground, understory, subcanopy, and canopy) and the routes along which we followed the groups. We then divided our data into two equivalent stages, randomized the data for each stage and looked for significant differences using Wilcoxon tests. Our results show a significant decrease in submissive behaviors toward the observer for both groups and a significant increase in resting and foraging for Group 1. In addition, Group 2 used the subcanopy significantly less and the understory more during the second stage. The routes the animals used were significantly longer in the second stage for Group 1, but not for Group 2. We conclude that our methodology is adequate to advance in the habituation of L. lagonotus in less than 2 months and that a group will habituate more quickly if it has had some previous neutral exposure to humans.

Contextual complexity of chemical signals in callitrichids.

In nearly four decades our research and that of others on chemical signaling in callitrichid primates suggest a high degree of contextual complexity in both the use of signals and the response to these signals. We describe our research including observational field studies, behavioral bioassays ("playbacks"), functional imaging, and conditioning studies. Scent marking in both captivity and the wild is used for more than just territorial marking. Social contextual effects are seen in responses by subordinate females responding with ovulatory inhibition only to chemical signals from familiar dominant reproductive females. Males detect ovulation through changes in scent marks. Males responded behaviorally and hormonally to chemical signals of novel ovulating females as a function of their reproductive status (fathers, males paired with a female but not fathers, and single males). Multiple brain areas are activated in males by female chemical signals of ovulation including areas relating to memory, evaluation, and motivation. Furthermore, males can be conditioned to respond sexually to a nonsexual odor demonstrating that learning plays an important role in response to chemical signals. Male androgen and estrone levels changed significantly in response to infant chemical signals as a function of whether the males were fathers or not, whether the odors were from their own versus other infants, as well as the infant's stage of development. Chemical signals in callitrichids are providing a rich source of understanding the context and function of the chemical sensory system and its stimulation of neural, behavioral, and hormonal actions in the recipients.

The role of food transfers in wild golden lion tamarins (Leontopithecus rosalia): Support for the informational and nutritional hypothesis.

Callitrichidae is a unique primate family not only in terms of the large number of food transfers to infants but also for the prevalence of transfers that are initiated by the adults. It has been hypothesized that, as well as provisioning infants, callitrichid food transfers might function to teach the receiver what food types to eat. If food provisioning has a teaching function, we would expect successful food transfers to be more likely with food types that are novel to the juveniles. We would also expect juveniles to learn about foods from those transfers. We introduced different types of food (some familiar, some novel) to wild groups of golden lion tamarins (Leontopithecus rosalia). While novel foods were not more successfully transferred than familiar food in the experiment, transfers were more successful (i.e., the receiver obtained food) when the donor had previous experience with that food. Moreover, we found evidence suggesting that food transfers influenced the future foraging choices of juveniles. Our findings are consistent with the first and third criteria of the functional definition of teaching, which requires that tutors (the adults) modify their behavior in the presence of a naïve individual (a juvenile), and that the naïve individual learns from the modified behavior of the demonstrator. Our findings are also consistent with the provisioning function of food transfer. Social learning seems to play an important role in the development of young tamarins' foraging preferences.

Intergroup food transfers in wild golden lion tamarins (Leontopithecus rosalia).

The transfer of food between adults is uncommon in primates. Although golden lion tamarins (Leontopithecus rosalia) are unique among primates in the extent to which they transfer food, reports of food transfers between adults have so far been restricted to captive or reintroduced individuals. Here, I report the first recorded events of adult-adult food transfers in golden lion tamarins between individuals belonging to different groups in the wild. Given that individuals emigrate from their natal group to find reproductive opportunities, I suggest that intergroup food transfers could be a way for individuals to estimate the quality or availability of potential mates or social partners. I propose an additional function of food transfers in wild golden lion tamarins: that they create and strengthen social bonds with individuals outside of the family group.

Abdominal ultrasound in Saguinus ursulus.

BACKGROUND: The classification of Saguinus ursulus as a new taxon and the vulnerability of this species highlighted the need for data on its specific morphophysiological attributes. This study used ultrasound to determine the typical characteristics of pelvic-abdominal structures and organs. METHODS: Nine healthy primates of the species S. ursulus were evaluated, through ultrasound tests, to determine the morphometry of the organs of the pelvic-abdominal cavity and the levels of ovarian activity. RESULTS: Topography, morphology, and biometrics of the organs were described. It was observed that organs of S. ursulus are similar to those of other Neotropical primate species. However, the kidney morphology is different,the left is triangular and the right is elliptical, while the gallbladder is bilobed. CONCLUSION: Ultrasonography has proven to be efficient and effective for organ evaluation. The ultrasound findings are a first step toward understanding the physiology of a less-known species.

Natural Transmission of Helicobacter saguini Causes Multigenerational Inflammatory Bowel Disease in C57/129 IL-10-/- Mice.

Cotton-top tamarins (CTTs) are an ideal model of human inflammatory bowel disease (IBD) because these animals develop multigenerational, lower bowel cancer. We previously isolated and characterized a novel enterohepatic Helicobacter species, Helicobacter saguini, from CTTs with IBD and documented that H. saguini infection in germfree C57BL IL-10-/- mice recapitulates IBD, suggesting that H. saguini influences IBD etiopathogenesis. In this study, we utilized a germfree IL-10-/- model to illustrate that H. saguini infection can naturally transmit and infect four generations and cause significant intestinal inflammatory pathology. Additionally, whole-genome sequencing of representative H. saguini isolates from each generation of IL-10-/- mice revealed gene mutations suggestive of multigenerational evolution. Overall, these results support that specific bacterial species with pathogenic potential, like H. saguini, are transmissible microorganisms in the etiopathogenesis of IBD in CTTs and reinforces the importance of specific microbiota in the pathogenesis of IBD in humans.IMPORTANCE While family history is a significant risk factor for developing inflammatory bowel disease (IBD), it is unclear whether the microbiome from parents is a transmissible influence on disease in their offspring. Furthermore, it is unknown whether IBD-associated microbes undergo genomic adaptations during multigenerational transmission and chronic colonization in their hosts. Herein, we show that a single bacterial species, Helicobacter saguini, isolated from a nonhuman primate species with familial IBD, is transmissible from parent to offspring in germfree IL-10-/- mice and causes multigenerational IBD. Additionally, whole-genome sequence analysis of H. saguini isolated from different mouse generations identified microevolutions in environmental interaction, nutrient metabolism, and virulence factor genes that suggest that multigenerational transmission may promote adaptations related to colonization and survival in new hosts and chronic inflammatory environments. The findings from our study highlight the importance of specific bacterial species with pathogenic potential, like H. saguini, as transmissible microorganisms in the etiopathogenesis of IBD.

Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species.

Seed dispersal distance (SDD) critically influences the survival of seedlings, spatial patterns of genetic diversity within plant populations, and gene flow among plant populations. In animal-dispersed species, foraging behavior and movement patterns determine SDD. Direct observations of seed dispersal events by animals in natural plant populations are mostly constrained by the high mobility and low visibility of seed dispersers. Therefore, diverse alternative methods are used to estimate seed dispersal distance, but direct comparisons of these approaches within the same seed dispersal system are mostly missing.We investigated two plant species with different life history traits, Leonia cymosa and Parkia panurensis, exclusively dispersed by two tamarin species, Saguinus mystax and Leontocebus nigrifrons. We compared SDD estimates obtained from direct observations, genetic identification of mother plants from seed coats, parentage analysis of seedlings/saplings, and phenomenological and mechanistic modeling approaches.SDD derived from the different methods ranged between 158 and 201 m for P. panurensis and between 178 and 318 m for L. cymosa. In P. panurensis, the modeling approaches resulted in moderately higher estimates than observations and genotyping of seed coats. In L. cymosa, parentage analysis resulted in a lower estimate than all other methods. Overall, SDD estimates for P. panurensis (179 ± 16 m; mean ± SD) were significantly lower than for L. cymosa (266 ± 59 m; mean ± SD).Differences among methods were related to processes of the seed dispersal loop integrated by the respective methods (e.g., seed deposition or seedling distribution). We discuss the merits and limitations of each method and highlight the aspects to be considered when comparing SDD derived from different methodologies. Differences among plant species were related to differences in reproductive traits influencing gut passage time and feeding behavior, highlighting the importance of plant traits on animal-mediated seed dispersal distance.

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.

Population Genetic Structure of an Endangered Endemic Primate (Leontopithecus chrysomelas) in a Highly Fragmented Atlantic Coastal Rain Forest.

This study evaluated the genetic structure of wild populations of the endangered primate, Leontopithecus chrysomelas. We tested the assumption that populations of L. chrysomelas, given their larger population size and a higher degree of habitat continuity, would have higher genetic diversity and less genetic structuring than other lion tamarins. We used 11 microsatellites and 122 hair samples from different locations to assess their genetic diversity and genetic structure, and to make inferences about the isolation by distance. The overall expected heterozygosity (0.51 ± 0.03) and the average number of alleles (3.6 ± 0.2) were relatively low, as is the case in other endangered lion tamarins. Genetic clustering analyses indicated two main clusters, whereas the statistical analyses based on genotype similarities and Fst suggested further substructure. A Mantel test showed that only 34% of this genetic differentiation was explained by the linear distance. In addition to linear distance, structural differences in the landscape, physical barriers and behavioural factors may be causing significant genetic structuring. Overall, this study suggests that these populations have a relatively low genetic diversity and a relatively high population genetic structure, putting in question whether the presence of agroforest systems (known locally as cabruca) is enough to fully re-establish functional landscape connectivity.

Next-Generation Sequencing of the Complete Mitochondrial Genome of the Endangered Species Black Lion Tamarin Leontopithecus chrysopygus (Primates) and Mitogenomic Phylogeny Focusing on the Callitrichidae Family.

We describe the complete mitochondrial genome sequence of the Black Lion Tamarin, an endangered primate species endemic to the Atlantic Rainforest of Brazil. We assembled the Leontopithecus chrysopygus mitogenome, through analysis of 523M base pairs (bp) of short reads produced by next-generation sequencing (NGS) on the Illumina Platform, and investigated the presence of nuclear mitochondrial pseudogenes and heteroplasmic sites. Additionally, we conducted phylogenetic analyses using all complete mitogenomes available for primates until June 2017. The single circular mitogenome of BLT showed organization and arrangement that are typical for other vertebrate species, with a total of 16618 bp, containing 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes, and 1 non-coding region (D-loop region). Our full phylogenetic tree is based on the most comprehensive mitogenomic dataset for Callitrichidae species to date, adding new data for the Leontopithecus genus, and discussing previous studies performed on primates. Moreover, the mitochondrial genome reported here consists of a robust mitogenome with 3000X coverage, which certainly will be useful for further phylogenetic and evolutionary analyses of Callitrichidae and higher taxa.

Food-Offering Calls in Wild Golden Lion Tamarins (Leontopithecus rosalia): Evidence for Teaching Behavior?

Many animals emit calls in the presence of food, but researchers do not always know the function of these calls. Evidence suggests that adult golden lion tamarins (Leontopithecus rosalia) use food-offering calls to teach juveniles which substrate (i.e., microhabitat) to forage on, or in, for food. However, we do not yet know whether juveniles learn from this aspect of the adults' behavior. Here we examine whether juveniles learn to associate food-offering calls with a foraging substrate, as a step toward assessing whether these calls qualify as teaching behavior. We compared the performance of four wild juvenile golden lion tamarins that were introduced to a novel substrate while exposed to playbacks of food-offering calls (experimental condition) to the performance of three juveniles that were exposed to the novel substrate without the presence of food-offering playbacks (control condition). We varied the location of the novel substrate between trials. We found that food-offering calls had an immediate effect on juveniles' interactions with the novel substrate, whether they inserted their hands into the substrate and their eating behavior, and a long-term effect on eating behavior at the substrate. The findings imply that juvenile golden lion tamarins can learn through food-offering calls about the availability of food at a substrate, which is consistent with (but does not prove) teaching in golden lion tamarins through stimulus enhancement. Our findings support the hypothesis that teaching might be more likely to evolve in cooperatively breeding species with complex ecological niches.

Ultrasonographic aspects of the Leontopithecus gestation (Lesson, 1840-Callitrichidae, Primates).

BACKGROUND: There is a concern about conservation of endangered species today. Among this species, the Leontopithecus (Lesson, 1840) is outstanding. Its population has been whirling reduced. So far the reproductive physiology of Leontopithecus has few studies, it is fundamental requisite to preserve this species. Obstetric sonography has become an essential method in reproductive management of primates. METHOD: This method is very helpful to detect early pregnancy and evaluate some deficiency of fetal growth. In this study, 14 pregnancies were monitored using real-time abdominal sonography. During each evaluation, the number of fetus was recorded, gestational sac and heart beats were observed, and biparietal diameter was measured. RESULTS: The results showed that abdominal sonography is a reliable method for observation of gross morphological changes during pre-natal development and to estimate gestational age. No statistically differences were observed between twins and singletons. This study is the first investigation of pre-natal growth in Leontopithecus.

Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines.

Since Darwin (), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's () theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, ; Heinsohn, ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, ).

Fatal Parastrongylus dujardini infection in captive callitrichids.

Intravascular nematodes were considered the cause of death of 14 captive callitrichids. All animals were captive born at zoos in France and died with little or no premonitory signs of disease. No consistent gross lesions were observed at necropsy, although in certain cases intracardiac adult parasites were noted. The most significant histologic findings were verminous pneumonia and pulmonary endarteritis. In all cases except one, intravascular adult nematodes were observed with eggs and larvae in the lungs. Adult nematodes were obtained from 8 animals and in all cases were identified as Parastrongylus dujardini. To the authors' knowledge, this is the first report of intravascular angiostrongylosis with primary cardiopulmonary location in callitrichids in France.

Nasal, oral and rectal microbiota of Black lion tamarins (Leontopithecus chrysopygus)

Black lion tamarins (Leontopithecus chrysopygus) are endangered callithrichids. Their conservation may require future translocations or reintroductions; however these approaches involve risks of pathogen introduction in the environment and stress-related opportunistic infections in these animals. In order to screen for opportunistic and potential pathogenic bacterial and fungal microbiota, ten free-ranging and ten captive Black lion tamarins were studied and the results compared. Nasal, oral and rectal swabs were collected and cultured for aerobic and facultative anaerobic bacteria and fungi, and a total 203 bacterial and 84 fungal isolates were obtained. Overall, the most frequent organisms were Staphylococcus spp., Bacillus spp., Candida spp. and Aspergillus spp. Microbiota of free-ranging and captive animals were similar in composition. A number of potentially pathogenic organisms were identified, emphasizing the importance of microbiological screening in future translocation or reintroduction conservation management programs.