Golden lion tamarin metapopulation dynamics five years after heavy losses to yellow fever.

The golden lion tamarin (GLT) is an Endangered primate endemic to Brazil's lowland Atlantic Forest. After centuries of deforestation and capture for the pet trade, only a few hundred individuals survived, all in isolated forest fragments 85 km from Rio de Janeiro city. Intensive conservation actions, including reintroduction of zoo-born tamarins, increased numbers to about 3700 in 2014. The most severe yellow fever epidemic/epizootic in Brazil in 80 years reduced two of the largest GLT populations by over 90%. Herein we report the results of a 2023 survey of GLTs designed to examine the dynamics of population recovery following yellow fever. Results indicate that populations hard hit by yellow fever are recovering due in part to immigration from adjacent forest fragments. No local extirpations were observed. About 4800 GLTs live in the survey area. This represents a 31% increase since the baseline survey completed in 2014. Two factors explain most of the increase: four large areas that had no GLTs or very low-density populations in 2014 are now at moderate density (three areas) or low density (one area), explaining 71% of overall increase since 2014. Increase in forest area within our survey area may explain up to 16% of the increase in GLT numbers since 2014. Results of computer simulations suggest that strengthening forest connectivity will facilitate metapopulation resilience in the face of mortality factors such as yellow fever.

Linking glucocorticoid variations to monthly and daily behavior in a wild endangered neotropical primate.

Identifying the factors swaying physiological stress levels in wild animals can help depict how they cope with environmental and social stressors, shedding light on their feeding ecology, behavioral plasticity, and adaptability. Here, we used noninvasive methods to explore the link between glucocorticoid levels and behavior in an endangered neotropical primate facing habitat fragmentation pressure, the black lion tamarin (Leontopithecus chrysopygus). We investigated monthly and day-to-day glucocorticoid variations independently to attempt to disentangle the complex nature of the adrenocortical activity. Between May 2019 to March 2020, we followed two groups of black lion tamarins in two different areas, a continuous forest and a small fragment, and gathered behavioral data (over 95 days in total; 8.6 ± 3.9 days/month) and fecal samples (Nsamples = 468; 4.93 ± 3.5 samples/day) simultaneously. Preliminary analyses enabled us to identify circadian variations linked to the biological rhythm, which were taken into account in subsequent models. Monthly analyses revealed that black lion tamarin fecal glucocorticoid metabolite levels vary according to changes in activity budget associated with the fruit consumption, movement, and resting time of the groups. At a day-to-day level, while intergroup encounters led to increases in fecal glucocorticoid metabolite concentrations, we found that changes in food intake or activity level did not trigger physiological stress responses. These findings suggest that diet and ranging patterns, driven by food availability and distribution, influence physiological stress at a seasonal scale, while acute stressors such as interspecific competition trigger short-term stress responses. Exploring fecal glucocorticoid metabolite variations over different timescales can help uncover the predictive and reactive facets of physiological stress in wild species. Moreover, having a comprehensive understanding of the physiological state of species is a valuable conservation tool for evaluating how they cope in changing environments.

Non-thrombotic pulmonary embolism of brain, liver, or bone marrow tissues associated with traumatic injuries in free-ranging neotropical primates.

From 2016 to 2019, Southeastern Brazil faced an outbreak of yellow fever (YF) affecting both humans and New World primates (NWP). The outbreak was associated with a marked increase in traumatic lesions in NWP in the affected regions. Non-thrombotic pulmonary embolization (NTPE) can be a consequence of massive traumatic events, and it is rarely reported in human and veterinary medicine. Here, we describe NTPE of the brain, liver, and bone marrow in free-ranging NWP, highlighting the epidemiological aspects of these findings and the lesions associated with this condition, including data on traumatic injuries in wild NWP populations during the course of a recent YF outbreak. A total of 1078 NWP were necropsied from January 2017 to July 2019. Gross traumatic injuries were observed in 444 marmosets (44.3%), 10 howler monkeys (23.2%), 9 capuchins (31.0%), 1 titi-monkey (50.0%), and 1 golden lion tamarin (33.3%). NTPE was observed in 10 animals, including 9 marmosets (2.0%) and 1 howler monkey (10.0%). NTPE was identified in the lung and comprised hepatic tissue in 1 case, brain tissue in 1 case, and bone marrow tissue in 8 cases. Although uncommon, it is important to consider NTPE with pulmonary vascular occlusion during the critical care of traumatized NWP. In addition, this study highlights the importance of conservational strategies and environmental education focusing on One Health, not only to protect these free-ranging NWP populations but also to maintain the efficacy of epidemiological surveillance programs.

Behavioral Implications of Enrichment for Golden Lion Tamarins: A Tool for Ex Situ Conservation.

The re-release of golden lion tamarins (Leontopithecus rosalia), from zoos into the wild, is considered to be an ex situ conservation success story. However, zoo-born golden lion tamarins have lower survival rates than their wild-born offspring, potentially due to deficient foraging and locomotion 'survival skills' acquired in captivity. The current study aimed to evaluate whether a puzzle feeder suspended and baited with different items could promote increased foraging and general activity in tamarins living in a zoo setting. A pair of tamarins at Woodland Park Zoo received the puzzle feeder in three conditions in an ABCACB experimental reversal design over a period of three months: an empty feeder and feeders baited with either fruit (raisins) or insects (mealworms). Food type affected behavior; time spent climbing increased when the feeder contained insects compared to fruit. Subjects interacted with the baited puzzle feeder device significantly more than the empty feeder, and use was highest within the first 30 minutes of exposure. Our results suggest that the puzzle feeders plus food were effective in increasing foraging and general activity.

Gastrointestinal parasites of Leontopithecus chrysomelas in the Atlantic Forest, Brazil / Parasitas gastrintestinais de Leontopithecus chrysomelas na Floresta Atlântica, Brasil

Abstract We performed coproparasitological testing of free-living golden-headed lion tamarins, Leontopithecus chrysomelas, using the Hoffmann-Pons-Janner method. In total, we collected 118 samples from ten groups: four living in Federal Protected Area and six living in Non-Protected Areas of cocoa farms. Eggs from parasites of the Acanthocephala phylum and Spiruridae, Ancylostomatidae, Ascarididae and Oxyuridae families were identified, as well as the genus Strongyloides (Nematode: Strongyloididae) and phylum Apicomplexa. This is the first description of infection with coccidian, Trichuridae family and Strongyloides spp. in L. chrysomelas. A total of 48% (n= 57) of the animals were infected and the highest prevalence (37.2±SD 8.72, n = 44) was for Acanthocephalidae, followed by Spiruridae (8.5±SD 5.03, n = 10). There was no difference in parasite prevalence by age classes or sex. However, we found higher diversity and prevalence of parasites in animals living in the Federal Protected Area. These results suggest that intestinal parasites may be influenced by environmental factors, such as the management of the areas where the animals live, in addition to the feeding behavior of L. chrysomelas and distinct transmission strategies of parasites. The combination of ecological and demographic data combined with parasitological studies may contribute to conservation programs for this species.

Resumo Foram realizados testes coproparasitológicos de micos-leões-dourados de vida livre, Leontopithecus chrysomelas, usando-se o método de Hoffmann-Pons-Janner. No total, foram coletadas 118 amostras de dez grupos: quatro grupos residentes em Área de Conservação Federal e seis grupos em Área não protegida de fazendas de cacau. Ovos de parasitas do filo Acantocephala e das famílias Spiruridae, Ancylostomatidae, Ascarididae, Oxyuridae foram identificados, bem como o gênero Strongyloides (Nematoda: Strongyloididae) e o filo Apicomplexa. Esta é a primeira descrição de infecção de coccídeos, família Trichuridae e Strongyloides spp. em L. chrysomelas. Um total de 48% (n = 57) dos animais estavam parasitados e a maior prevalência (37,2 ±DP 8,72, n = 44) foi para Acanthocephalan, seguido por Spiruridae (8,5±DP 5,03, n = 10). Não houve diferença na prevalência do táxon de parasita por idade ou sexo. No entanto, foi encontrada maior diversidade e prevalência de parasitas em animais que vivem na Unidade de Conservação Federal. Esses resultados sugerem que os parasitas intestinais podem ser influenciados por fatores ambientais, como o manejo das áreas, além do comportamento alimentar de L. chrysomelas e distintas estratégias de transmissão dos parasitas. A combinação de dados ecológicos e demográficos com estudos parasitológicos podem contribuir para programas de conservação dessa espécie.

The mitochondrial genome and Epigenome of the Golden lion Tamarin from fecal DNA using Nanopore adaptive sequencing.

BACKGROUND: The golden lion tamarin (Leontopithecus rosalia) is an endangered Platyrrhine primate endemic to the Atlantic coastal forests of Brazil. Despite ongoing conservation efforts, genetic data on this species remains scarce. Complicating factors include limitations on sample collection and a lack of high-quality reference sequences. Here, we used nanopore adaptive sampling to resequence the L. rosalia mitogenome from feces, a sample which can be collected non-invasively. RESULTS: Adaptive sampling doubled the fraction of both host-derived and mitochondrial sequences compared to sequencing without enrichment. 258x coverage of the L. rosalia mitogenome was achieved in a single flow cell by targeting the unfinished genome of the distantly related emperor tamarin (Saguinus imperator) and the mitogenome of the closely related black lion tamarin (Leontopithecus chrysopygus). The L. rosalia mitogenome has a length of 16,597 bp, sharing 99.68% sequence identity with the L. chrysopygus mitogenome. A total of 38 SNPs between them were identified, with the majority being found in the non-coding D-loop region. DNA methylation and hydroxymethylation were directly detected using a neural network model applied to the raw signal from the MinION sequencer. In contrast to prior reports, DNA methylation was negligible in mitochondria in both CpG and non-CpG contexts. Surprisingly, a quarter of the 642 CpG sites exhibited DNA hydroxymethylation greater than 1% and 44 sites were above 5%, with concentration in the 3' side of several coding regions. CONCLUSIONS: Overall, we report a robust new mitogenome assembly for L. rosalia and direct detection of cytosine base modifications in all contexts.

Integrating climate and landscape models to prioritize areas and conservation strategies for an endangered arboreal primate.

Species distributions are influenced by both climate conditions and landscape structure. Here we propose an integrated analysis of climatic and landscape niche-based models for a forest-dependent primate, the endangered black lion tamarin (Leontopithecus chrysopygus). We applied both climate and landscape variables to predict the distribution of this tamarin and used this information to prioritize strategic areas more accurately. We anticipated that this approach would be beneficial for the selection of pertinent conservation strategies for this flagship species. First, we built climate and landscape niche-based models separately, combining seven algorithms, to infer processes acting on the species distribution at different scales. Subsequently, we combined climate and landscape models using the EcoLand Analysis. Our results suggest that historic and current landscape fragmentation and modification had profoundly adverse effects on the distribution of the black lion tamarins. The models indicated just 2096 km2 (out of an original distribution of 92,239 km2 ) of suitable areas for both climate and landscape. Of this suitable area, the species is currently present in less than 40%, which represents less than 1% of its original distribution. Based on the combined map, we determined the western and southeast regions of the species range to be priority areas for its conservation. We identified areas with high climatic and high landscape suitability, which overlap with the remaining forest fragments in both regions, for habitat conservation and population management. We suggest that areas with high climatic but low landscape suitability should be prioritized for habitat management and restoration. Areas with high landscape suitability and low climatic suitability, such as the Paranapiacaba mountain range should be considered in light of projected climate change scenarios. Our case study illustrates that a combined approach of climatic and landscape niche-based modeling can be useful for establishing focused conservation measures that may increase the likelihood of success.

Malassezia japonica is part of the cutaneous microbiome of free-ranging golden-headed lion tamarins (Leontopithecus chrysomelas - Kuhl, 1820).

We investigated Malassezia spp. in external ear canal and haircoat of free-ranging golden-headed lion tamarins (Leontopithecus chrysomelas). A total of 199 animals were restrained, and 597 clinical samples were collected. After the amplification of the 26S ribosomal gene by polymerase chain reaction (PCR), the RFLP technique was performed. Two additional PCR protocols were performed in 10 randomly selected strains. Malassezia sp. was isolated in 38.2% (76/199) of the animals and 14.6% (87/597) of the samples; all strains were lipodependent. The 10 sequenced strains showed a high identity with Malassezia japonica, species described in man, but not in animals, so far.

Genetic assessment for the endangered black lion tamarin Leontopithecus chrysopygus (Mikan, 1823), Callitrichidae, Primates.

This is the first study analyzing genetic diversity in captive individuals of the endangered black lion tamarin, Leontopithecus chrysopygus, and also comparing genetic diversity parameters between wild populations and captive groups using the same set of molecular markers. We evaluated genetic diversity and differentiation for the Brazilian and European captive groups and a wild population through 15 polymorphic microsatellite markers. The genetic diversity levels were similar among Brazilian captive, European captive and wild animals from the National Forest of Capão Bonito. Expected heterozygosity showed values ranging from 0.403 to 0.462, and significant differences were not observed among the populations. Different allele frequencies were observed among the groups, which showed the presence of distinct private alleles. The PCoA analysis evidenced three main clusters suggesting that the captive Brazilian and European groups are markedly differentiated both from one another and from the wild population of Capão Bonito. Likewise, the most likely number of genetic clusters (K) revealed by Structure was three. Such a structure is probably the result of the strength of drift and non-random reproduction in these small and isolated groups. Despite this differentiation, all groups still have similar genetic diversity levels, comparable to other callitrichids. The data obtained herein are important to increasing knowledge of the genetics of tamarins and supporting breeding programs to prevent loss of genetic diversity and inbreeding depression.

TREATMENT OF DIABETES MELLITUS IN A GOLDEN LION TAMARIN (LEONTOPITHECUS ROSALIA) WITH THE GLUCAGON-LIKE PEPTIDE-1 MIMETIC EXENATIDE.

An 8-yr-old male golden lion tamarin ( Leontopithecus rosalia ) was diagnosed with diabetes mellitus based on hyperglycemia and persistent glycosuria. Initial treatment consisted of the oral antihyperglycemic medications glipizide and metformin that resulted in decreased blood glucose concentrations; however, marked glycosuria persisted. Insufficient improvement on oral antihyperglycemic therapy and poor feasibility of daily subcutaneous insulin therapy led to an investigation into an alternative therapy with extended-release exenatide, a glucagon-like peptide-1 (GLP-1) mimetic, at a dosage of 0.13 mg/kg subcutaneously once per month. Following treatment with exenatide, the persistent glycosuria resolved, the animal maintained normal blood glucose concentrations, and had lower serum fructosamine concentrations compared to pretreatment levels. Based on these findings, extended-release exenatide could be considered as a therapeutic option in nonhuman primates with diabetes mellitus that do not respond to oral antihyperglycemics and in which daily subcutaneous insulin is not feasible.

HEPATIC OSTEODYSTROPHY IN A GOLDEN LION TAMARIN (LEONTOPITHECUS ROSALIA).

An 8-yr-old, captive, female golden lion tamarin ( Leontopithecus rosalia ) with a 6-yr history of hyperbilirubinemia was examined for inappetence and weight loss. Physical examination and blood pressure monitoring under anesthesia revealed hypothermia and hypotension, and blood work revealed hypoglycemia, markedly elevated liver enzymes, including serum alkaline phosphatase, aspartate aminotransferase, and alanine aminotransferase, and confirmed the hyperbilirubinemia. A complete blood count suggested chronic lymphoid leukemia. The animal's condition deteriorated during recovery, and the animal died despite aggressive treatment. Grossly, there was micronodular cirrhosis of the liver, severe icterus, and diffuse osteopenia of all examined bones. Microscopic examination of the liver confirmed the micronodular cirrhosis and bone lesions were compatible with diffuse osteopenia and osteomalacia. This brief communication presents a case of chronic liver disease and lesions indicative of metabolic bone disease, also known as hepatic osteodystrophy. To the authors' knowledge, this is the first documented case of hepatic osteodystrophy in the veterinary literature.

Diurnal frugivores on the Bromeliaceae Aechmea depressa L.B. Sm. from Northeastern Brazil: the prominent role taken by a small forest primate / Frugívoros diurnos de Aechmea depressa L.B. Sm. (Bromeliaceae) do Nordeste do Brasil e o papel proeminente de um pequeno primata florestal

Little is known about frugivory of epiphytes. We investigated diurnal frugivores consuming Aechmea depressa, an endemic species from Southern Bahia, Brazil, through 67 hours of observation on three fruiting individuals. Infructescences were visited for 2 percent of the time and only by golden-headed lion tamarins (GHLTs; Leontopithecus chrysomelas). Aechmea depressa invests on physical defense to retain fruits for prolonged periods, however, GHLTs used their small size and dexterity to remove rigid bracts and extract fruits from the infructescence. Prior studies indicate GHLTs disperse Aechmea seeds. Given the low visitation rates and probability that few frugivores successfully manipulate A. depressa fruits, we suggest that GHLTs are extremely important to maintaining the populations of this bromeliad species.

Pouco se sabe sobre a frugivoria em plantas epífitas. Nós investigamos os frugívoros diurnos de Aechmea depressa, uma espécie endêmica do Sul da Bahia através de 67 horas de observação dos frutos de três indivíduos. As infrutescências foram visitadas em 2 por cento do tempo somente por micos-leão-da-cara-dourada (MLCD; Leontopithecus chrysomelas). Aechmea depressa investe na defesa física para reter seus frutos por períodos prolongados entretanto, o MLCD utiliza seu pequeno tamanho e extrema destreza para remover as brácteas rígidas e extrair os frutos da infrutescência. Estudos prévios indicam que os MLCDs dispersam sementes de espécies de Aechmea. Baseando-se na baixa taxa de visitação e na probabilidade de que poucos frugívoros manipulem adequadamente os frutos de A. depressa, nós sugerimos que os MLCD sejam extremamente importantes para manter as populações desta espécie de Bromeliaceae.

Morfologia macroscópica do aparelho reprodutor feminino de Leontopithecus cativos (Lesson, 1840) Primates-Callitrichidae / Gross morphology of the female genital tract of captive Leontopithecus (Lesson, 1840) Primates-Callitrichidae

Descreveu-se o sistema reprodutor feminino em três espécies de mico-leão Leontopithecus (Lesson 1840), cativos: L. rosalia, L. chrysopygus e L. chrysomelas. A vulva está delimitada pelos lábios vulvares menores e com clitóris conspícuo. A superfície do períneo urogenital apresenta elevações papilares mais concentradas nos lábios vulvares, conferindo-lhe aspecto rugoso. O vestíbulo vaginal constitui um tubo muscular de parede espessa que se estende da rima da vulva até o óstio da vagina. A vagina é um tubo muscular alongado e achatado dorsoventralmente, que comunica o vestíbulo vaginal ao colo uterino. O útero piriforme está localizado na porção caudal da cavidade abdominal. Craniolateralmente abrem-se tubas uterinas convolutas e ovários grosseiramente fusiformes de superfície lisa.

It is described the female genital tract of three species of lion tamarin: Leontopithecus rosalia, L. chrysopygus, and L. chrysomelas. Fifteen animals were selected from the Museum of the Center of Primatology of Rio de Janeiro - CPRJ/FEEMA. The vulva is delimited by the labia and has a conspicuous clitoris. The surface of the urogenital perineum has papillary elevations more concentrated in the labia, which results in a rough aspect. The vestibule is a thick-walled muscular tube, extending from the pudendal cleft to the vaginal orifice. The vagina is an elongated and flat muscular tube, which communicates dorsoventrally the vestibulum and the cervix of uterus. The pyriform uterus is located in the caudal portion of the abdominal cavity. Craniolaterally, the convolute uterine tubes open, enveloping the ovaries, which are roughly fusiform with a smooth surface.

Frugivory and seed dispersal of golden lion tamarin (Leontopithecus rosalia (Linnaeus, 1766)) in a forest fragment in the Atlantic Forest, Brazil / Frugivoria e dispersão de sementes por Micos-Leões-Dourados (Leontopithecus rosalia) em um fragmento florestal na Mata Atlântica, Brasil

The influence of the golden lion tamarin (Leontopithecus rosalia) as a seed disperser was studied by monitoring two groups of tamarins from December 1998 to December 2000 (871.9 hours of observations) in a forest fragment in south-east Brazil. The tamarins consumed fruits of 57 species from at least 17 families. They ingested the seeds of 39 species, and 23 of these were put to germinate in the laboratory and/or in the field. L. rosalia is a legitimate seed disperser because the seeds of all species tested germinated after ingestion, albeit some in low percentages. These primates do not show a consistent effect in final seed germination, because they benefit some species while damaging others. Feces were examined for seeds that had been preyed upon or digested.

A influência do mico-leão-dourado (Leontopithecus rosalia) como dispersor de sementes foi estudada através do monitoramento de dois grupos de micos de dezembro de 1998 a dezembro de 2000 (871,9 horas de observações) em um fragmento florestal no Sudeste do Brasil. Os micos consumiram frutos de 57 espécies de pelo menos 17 famílias. Eles ingeriram sementes de 39 espécies, e 23 destas foram colocadas para germinar no laboratório e/ou no campo. L. rosalia é um dispersor de sementes legítimo porque sementes de todas as espécies testadas germinaram após a ingestão, mesmo que em baixas porcentagens. Esses primatas não apresentam um efeito consistente na germinação final de sementes, porque beneficiam algumas espécies enquanto prejudicam outras. Sementes predadas ou digeridas foram procuradas nas fezes.

Correlates of molt in golden lion tamarins (Leontopithecus rosalia).

In this paper we describe the timing and correlates of molt for a native population of golden lion tamarins (Leontopithecus rosalia). We conducted 820 examinations of 267 adult tamarins over a 7.75 year period to determine the annual molting cycle in this population. Dorsal molt was an annual event for most individuals in the study population; however, 10% of sampled individuals apparently molted twice in a 12 month period. Duration of molt was estimated at 5-6 weeks. The proportion of samples in which tamarins were in molt was significantly greater during the wet season than the dry season and positively correlated with mean monthly precipitation and minimum temperature but not tamarin births, suggesting an environmental component to timing of molt. We found no sex differences in the occurrence of molt during wet or dry seasons. However, the relative frequency of samples in molt was significantly less for gravid females than for nongravid females. In four polygynous groups, socially dominant females gave birth before subordinate females, and younger reproductive females completed molt before older reproductive females. © 1995 Wiley-Liss, Inc.

Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia).

Data on the ecology, demography, and morphology of 465 golden lion tamarins in 22 wild groups suggest that avoidance of reproduction and weaning of infants during the dry season shaped the pattern of female reproduction. Post-partum estrus may have evolved to allow females to produce and wean two successive litters during the 7-month season of abundant food resources. Support for these hypotheses includes observations that nearly all births, lactation, and weaning of infants occurred during the wet season, a period of relatively abundant trophic resources. Litter sizes in the wild were smaller than for the captive population. Evidence that food limitation may have a greater negative impact on young juveniles than lactating females includes observations that female weight did not decrease with lactation, and that many births occurred during the transition between dry and wet seasons. Juveniles gained less weight during the dry season than during the wet season; however, there was no significant difference between weights of adults born early vs. late in the wet season. For females producing two litters/year, litter size and infant mortality did not differ for litters born early and late in the wet season. Adult males gained weight before and lost weight during the month of highest probability of female estrus, suggesting that competition for mates is energetically expensive for males. Although resources were abundant, adult males did not gain weight during months when most infant carrying took place, suggesting that this activity is also energetically expensive. © 1994 Wiley-Liss, Inc.