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.

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.

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.

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.

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.

Informative microsatellites for genetic population studies of black-faced lion tamarins (Leontopithecus caissara).

Leontopithecus caissara is a critically endangered primate species from the Brazilian Atlantic Forest. Nineteen microsatellite loci, previously developed for congeneric species, were tested with 34 L. caissara individuals from Superagüi Island. Of the 19 loci, 17 (89.4%) produced robust alleles, nine (47.4%) of these proved to be polymorphic, with a total of 23 alleles and an average of 2.56 alleles per locus. Expected and observed heterozygosity averaged 0.483 and 0.561, respectively. The exclusion power for identifying the first parent of an arbitrary offspring was 0.315 over all loci. The results thus indicate both the usefulness and limitations of these nine microsatellite loci in the genetic analysis of L. caissara, as well as their potentiality for genetic investigation in other congeneric species.

Informative microsatellites for genetic population studies of black-faced lion tamarins (Leontopithecus caissara)

Leontopithecus caissara is a critically endangered primate species from the Brazilian Atlantic Forest. Nineteen microsatellite loci, previously developed for congeneric species, were tested with 34 L. caissara individuals from Superagüi Island. Of the 19 loci, 17 (89.4 percent) produced robust alleles, nine (47.4 percent) of these proved to be polymorphic, with a total of 23 alleles and an average of 2.56 alleles per locus. Expected and observed heterozygosity averaged 0.483 and 0.561, respectively. The exclusion power for identifying the first parent of an arbitrary offspring was 0.315 over all loci. The results thus indicate both the usefulness and limitations of these nine microsatellite loci in the genetic analysis of L. caissara, as well as their potentiality for genetic investigation in other congeneric species.

Ocorrência de Acanthocephala em Leontopithecus (Lesson, 1840), cativos: aspectos clínico-patológicos. Callitrichidae-Primates / Acanthocephala infections in captives lion tamarins Leontopithecus (Lesson, 1840): clinical pathologic aspects. Callitrichidae-Primates

Estudaram-se achados de necropsia de 454 espécimens de Leontopithecus. Quatorze (3,1 por cento) apresentaram-se infectados por acantocéfalos intestinais identificados como Prosthenorchis elegans (Diesing, 1861). Não foram observadas diferenças na ocorrência do parasito quanto à espécie, origem - cativos ou selvagens - e sexo. Clinicamente os animais apresentaram-se com o pelame eriçado, apatia, inapetência, dores abdominais e diarréia. Em dois animais parasitados (14,2 por cento), observou-se perfuração da parede intestinal. As lesões encontradas caracterizaram-se por uma grave enterite ulcerativa. A ocorrência desses parasitos reforça a necessidade do estabelecimento de protocolos sanitários rígidos no manejo das espécies de primatas do neotrópico

This study assessed the autopsy findings of 454 Leontopithecus specimens, 14 of which (3.1 percent) were infected by intestinal Acanthocephala identified as Prosthenorchis elegans (Diesing, 1861). No difference in the occurrence of the parasite was observed regarding the species, origin (captive or wild) and sex of the lion tamarins. Clinically, the animals had spiked coat, apathy, inappetence, abdominal pain and diarrhea. Two of the parasitized animals (14.2 percent) had perforation of the intestinal wall. The lesions found were characterized as a severe ulcerative enteritis. The occurrence of such parasites highlights the need for establishing strict sanitary protocols for the management of the neotropical primate species

Reproduction in captive lion tamarins (Leontopithecus): Seasonality, infant survival, and sex ratios.

Diversity in reproductive and social systems characterizes the primate family Callitrichidae. This paper contributes to our appreciation of this diversity by presenting the first detailed comparative analysis of captive breeding in three species of lion tamarins (Leontopithecus chrysomelas, L. chrysopygus, and L. rosalia) housed at the Centro de Primatologia do Rio de Janeiro. The annual pattern of reproduction in all three species of Leontopithecus was markedly seasonal, with births occurring during the spring, summer, and fall months from August through March. While modal number of litters produced per female per year was 1, approximately 20% of breeding females produced two litters per year. The onset of breeding activity in years when two litters are produced was significantly earlier than in years when only one litter was produced. The cumulative number of offspring surviving to 3 months of age did not differ between years with one vs. two breeding attempts. Like other callitrichids, postnatal mortality was highest during the first week of life, and there were pronounced species differences in offspring survival through 1 year, with significantly lower survivorship in L. chrysomelas. Infant survivorship was affected by a number of experiential factors. Survivorship up to 30 days of life was higher in groups in which the breeding female had previous experience with infants as a nonbreeding helper than in groups in which the female lacked previous helping experience. Likewise, survivorship to 30 days of life was higher for infants born to multiparous females than for infants born to primiparous females. When parity and previous helping experience were analyzed concurrently, the lowest survivorship was associated with offspring produced by inexperienced primiparous females. Genus-wide, there was no significant departure from a 50:50 sex ratio at any point during the first year of life, nor was there evidence for differential mortality for male and female infants. However, L. chrysopygus produced significantly more male infants at birth (65:44) and had male-biased litters (approximately 60% males) throughout the first year of life, while L. chrysomelas showed a nonsignificant tendency toward female-biased litters. © 1996 Wiley-Liss, Inc.

Acoustic structure of long calls in free-ranging groups of golden lion tarnarins, Leontopithecus rosalia.

Like many other callitrichids, golden lion tamarins, Leontopithecus rosalia, emit Long Calls. Recordings of four free-ranging groups were made to explore different types of Long Calls. Three Long Call types were identified acoustically, and analyzed sonographically. The calls usually started with an Introductory Syllable (a chirp, a trill, or a whine) which was followed by either one, two, or three different phrases in a fixed sequential order. Each of the three phrases was unique and contained a typical number of syllables of characteristic shape, frequencies, and durations. Possible functions of these calls are discussed. © 1994 Wiley-Liss, Inc.

Sex differences in vocal structure in a callitrichid primate, Leontopithecus rosalia.

Four types of calls (long calls, chirps, chucks, and trills) from Golden Lion Tamarins (Leontopithecus rosalia) were analyzed for sex differences in structure. Six or more acoustic variables were analyzed for each call type. One or more variables from each call category differed significantly between the sexes. In addition, discriminant function analyses were conducted on male vs. female data for each call type. Long calls, chirps, and chucks from males and females were quite discriminable, but trills were not. That these differences exist is surprising given that callitrichid primates are otherwise quite monomorphic in structure and behavior. Possible functions served by sex differences in call structure include group censusing or assessing the sex of transient individuals.