Epidemiologic profile and histopathological findings in Neotropical Primates during and after the yellow fever outbreak in Espírito Santo, Brazil.

Yellow fever (YF) is a viral disease whose transmission involves non-human primates (NHP), mosquitoes, and humans. Between 2016 and 2018 occurred the largest YF outbreak in the last 100 years in Brazil. We analyzed epidemiologic profile and geographic distribution of epizootics and described most frequent histopathological findings in NHP that died during YF outbreak in the state of Espírito Santo. We consider 487 epizootics notifications registered at the State Health Department from January 2017 to July 2020. Throughout the state, 51 (65.4%) municipalities reported epizootics, with more cases in central and metropolitan areas. Reverse transcription polymerase chain reaction and immunohistochemistry were laboratory tests performed for diagnosis of yellow fever, with 160 (32.9%) positive results, 314 (64.5%) negative and 13 (2.7%) inconclusive. Histopathological findings were compared statistically between positive and negative animals for YF. The liver was the most affected organ. Hemorrhage, hepatocyte necrosis, steatosis, cholestasis and eosinophilic degeneration were statistically more frequent in positive animals. Tubular necrosis, nephritis, congestion and lymphoid hypoplasia on spleen were statistically correlated to positive animals. Knowledge of pathogenic aspect of YF is necessary to guarantee that samples from Neotropical primates are properly used for YF surveillance purposes, to ensure appropriate diagnoses and subsequent public health responses.

Vasectomy of golden-headed lion tamarins (Leontopithecus chrysomelas) using local anesthesia after sedation with dexmedetomidine-ketamine-meperidine.

The study evaluated the combination of ketamine, dexmedetomidine, and meperidine for vasectomy in golden-headed lion tamarins. Lidocaine infiltration was required for intraoperative analgesia and atipamezole was used at the end of the procedure. The protocol promoted satisfactory sedation and analgesia with a short recovery time in tamarins.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

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.

Eco-Epidemiological Profile and Molecular Characterization of Simian Foamy Virus in a Recently-Captured Invasive Population of Leontopithecus chrysomelas (Golden-Headed Lion Tamarin) in Rio de Janeiro, Brazil.

Simian foamy viruses (SFV) infect a wide range of Old World and Neotropical primates (NP). Unlike Old World primates, little is known about the diversity and prevalence of SFV in NP, mainly from a free-living population. Phylogenetic analyses have shown that SFV coevolved with their hosts. However, viral strains infecting Leontopithecus chrysomelas did not behave as expected for this hypothesis. The purpose of this study was to determine the eco-epidemiological profile and molecular characterization of SFV in a recently captured invasive population of L. chrysomelas located in Niteroi/RJ using buccal swab as an alternative collection method. A prevalence of 34.8% (32/92) and a mean viral load of 4.7 log copies of SFV/106 cells were observed. With respect to time since capture, SFV prevalence was significantly higher in the group of animals sampled over 6 months after capture (55.2%) than in those more recently captured (25.4%) (p = 0.005). Infected solitary animals can contribute to SFV transmission between different groups in the population. SFV strains formed two distinct clades within the SFV infecting the Cebidae family. This is the first study to use buccal swabs as a tool to study SFV diversity and prevalence in a recently free-living NP population upon recent capture.

Spontaneous meningoencephalitis by Staphylococcus aureus in an infant golden-headed lion tamarin (Leontopithecus chrysomelas).

Non-human primates are susceptible to many bacteria, some of which bear zoonotic potential. We report the pathologic features of spontaneous fulminating meningoencephalitis by Staphylococcus aureus in a captive infant golden-headed lion tamarin (Leontopithecus chrysomelas) from Brazil.

ATLANTIC-PRIMATES: a dataset of communities and occurrences of primates in the Atlantic Forests of South America.

Primates play an important role in ecosystem functioning and offer critical insights into human evolution, biology, behavior, and emerging infectious diseases. There are 26 primate species in the Atlantic Forests of South America, 19 of them endemic. We compiled a dataset of 5,472 georeferenced locations of 26 native and 1 introduced primate species, as hybrids in the genera Callithrix and Alouatta. The dataset includes 700 primate communities, 8,121 single species occurrences and 714 estimates of primate population sizes, covering most natural forest types of the tropical and subtropical Atlantic Forest of Brazil, Paraguay and Argentina and some other biomes. On average, primate communities of the Atlantic Forest harbor 2 ± 1 species (range = 1-6). However, about 40% of primate communities contain only one species. Alouatta guariba (N = 2,188 records) and Sapajus nigritus (N = 1,127) were the species with the most records. Callicebus barbarabrownae (N = 35), Leontopithecus caissara (N = 38), and Sapajus libidinosus (N = 41) were the species with the least records. Recorded primate densities varied from 0.004 individuals/km2 (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km2 (Alouatta caraya in Santiago, Rio Grande do Sul, Brazil). Our dataset reflects disparity between the numerous primate census conducted in the Atlantic Forest, in contrast to the scarcity of estimates of population sizes and densities. With these data, researchers can develop different macroecological and regional level studies, focusing on communities, populations, species co-occurrence and distribution patterns. Moreover, the data can also be used to assess the consequences of fragmentation, defaunation, and disease outbreaks on different ecological processes, such as trophic cascades, species invasion or extinction, and community dynamics. There are no copyright restrictions. Please cite this Data Paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.

Hematological evaluation of free-living golden-headed lion tamarins (Leontopithecus chrysomelas) from an Urban Atlantic Forest.

BACKGROUND: The Atlantic Forest where the animals were captured is surrounded by residences, so this close contact could favor the presence of disease-transmitting pathogens, putting the local population at risk. For these and other factors, it is important to perform laboratory tests enabling the performance of important diagnoses. METHODS: Blood samples of 268 golden-headed lion tamarins (Leontopithecus chrysomelas) inhabiting an Atlantic Forest area in Rio de Janeiro, Brazil, were processed for accessing age and sex influence in hematological parameters and to establish normative hematology values. RESULTS: Mean values of red blood cells, hematocrit, hemoglobin, and platelet count were significantly higher in adult males than in adult females. Adult animals had significantly higher mean neutrophil count, and young animals had higher averages than adults in lymphocyte values. Anisocytosis and platelet indices parameters were also provided for the first time. CONCLUSIONS: Averages presented can be used as hematological parameters for golden-headed lion tamarins.

Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation.

Primates occur in 90 countries, but four-Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC)-harbor 65% of the world's primate species (439) and 60% of these primates are Threatened, Endangered, or Critically Endangered (IUCN Red List of Threatened Species 2017-3). Considering their importance for global primate conservation, we examine the anthropogenic pressures each country is facing that place their primate populations at risk. Habitat loss and fragmentation are main threats to primates in Brazil, Madagascar, and Indonesia. However, in DRC hunting for the commercial bushmeat trade is the primary threat. Encroachment on primate habitats driven by local and global market demands for food and non-food commodities hunting, illegal trade, the proliferation of invasive species, and human and domestic-animal borne infectious diseases cause habitat loss, population declines, and extirpation. Modeling agricultural expansion in the 21st century for the four countries under a worst-case-scenario, showed a primate range contraction of 78% for Brazil, 72% for Indonesia, 62% for Madagascar, and 32% for DRC. These pressures unfold in the context of expanding human populations with low levels of development. Weak governance across these four countries may limit effective primate conservation planning. We examine landscape and local approaches to effective primate conservation policies and assess the distribution of protected areas and primates in each country. Primates in Brazil and Madagascar have 38% of their range inside protected areas, 17% in Indonesia and 14% in DRC, suggesting that the great majority of primate populations remain vulnerable. We list the key challenges faced by the four countries to avert primate extinctions now and in the future. In the short term, effective law enforcement to stop illegal hunting and illegal forest destruction is absolutely key. Long-term success can only be achieved by focusing local and global public awareness, and actively engaging with international organizations, multinational businesses and consumer nations to reduce unsustainable demands on the environment. Finally, the four primate range countries need to ensure that integrated, sustainable land-use planning for economic development includes the maintenance of biodiversity and intact, functional natural ecosystems.

Negative serosurvey of Toxoplasma gondii antibodies in Golden-headed Lion Tamarin (Leontopithecus chrysomelas) from Niterói/RJ, Brazil / Pesquisa sorológica de anticorpos anti-Toxoplasma gondii em Mico-leão-da-cara-dourada (Leontopithecus chrysomelas) de Niterói/RJ, Brasil

Abstract New World Nonhuman Primates are highly susceptible to clinical toxoplasmosis. Serum samples from 126 recently captured Leontopithecus chrysomelas, from an exotic and invasive population, were tested for Toxoplasma gondii antibodies by the modified agglutination test (MAT, cut-off 1:25); all were seronegative. The MAT is highly specific and is not species-specific. This is the first report of T. gondii survey in this tamarin in the wild. This result is consistent with prior reports that showed the high susceptibility of the species to infection by T. gondii usually with high mortality rates.

Resumo Primatas não humanos são extremamente susceptíveis a toxoplasmose. No presente estudo, 126 Leontopithecus chrysomelas foram capturados de uma população de vida livre, exótica e invasora, e amostras de soros foram testadas para a presença de anticorpos anti- Toxoplasma gondii pelo Teste de Aglutinação Modificado (MAT, ponto de corte 1:25). Todos os animais testados foram negativos. O MAT é um teste altamente específico e não é espécie-específico. Esse é o primeiro estudo de pesquisa por anticorpos anti- T. gondii nessa espécie em vida livre. O resultado corrobora com o conhecimento prévio sobre a susceptibilidade dessa espécie a infecção pelo parasite T. gondii.

Negative serosurvey of Toxoplasma gondii antibodies in Golden-headed Lion Tamarin (Leontopithecus chrysomelas) from Niterói/RJ, Brazil.

New World Nonhuman Primates are highly susceptible to clinical toxoplasmosis. Serum samples from 126 recently captured Leontopithecus chrysomelas, from an exotic and invasive population, were tested for Toxoplasma gondii antibodies by the modified agglutination test (MAT, cut-off 1:25); all were seronegative. The MAT is highly specific and is not species-specific. This is the first report of T. gondii survey in this tamarin in the wild. This result is consistent with prior reports that showed the high susceptibility of the species to infection by T. gondii usually with high mortality rates.

Seed Dispersal of Threatened Tree Species by a Critically Endangered Primate in a Brazilian Hotspot.

In the northern Atlantic Forest, hunting and habitat loss have eliminated most large mammals that disperse zoochoric fruits. Due to the decrease in populations of large seed dispersers, yellow-breasted capuchins (Sapajusxanthosternos) are currently one of the largest arboreal fruit-eating mammals in the region. During 26 months, we followed 14-25 capuchins aiming to (1) present data on their dietary ecology, (2) verify the conservation status of plants in the diet, and (3) determine distance and habitat of seed deposition based on gut retention time. Capuchins showed a preference for feeding in old secondary forests in spite of the greater availability of primary forests. They fed on 109 species of fruits (42.7% of feeding frequency) and swallowed 85 species of seeds (mean width: 0.73 ± 0.57 cm; mean length: 1.17 ± 0.83 cm). Capuchins consumed mostly oil palm and manilkara fruits. We observed long distances of seed deposition (median 300-360 m); 36.8-41.7% of these events occurred in a distinct habitat, and seeds of 12 late-stage trees swallowed in the primary forest were deposited in old secondary forests. S. xanthosternos has an important role in the first phase of seed dispersal (seed removal from the parent tree and seed deposition), particularly for 23 endemic and 3 endangered plants.

Hunting, pet trade, and forest size effects on population viability of a critically endangered Neotropical primate, Sapajus xanthosternos (Wied-Neuwied, 1826).

The yellow-breasted capuchin monkey (Sapajus xanthosternos) is one of the seven Brazilian primates that are currently threatened with extinction. Although the species is known to be threatened by habitat loss, hunting, and illegal pet trade, few data exist on how these threats influence its long-term population persistence. We conducted population viability analyses (PVAs) to estimate minimum viable populations of S. xanthosternos under 10 threat scenarios (i.e., varying hunting pressure and varying number of infants captured for the pet trade) for five forest fragments with different estimated carrying capacities (K). We also estimated the minimum forest fragment size required to sustain viable populations living under the same 10 threat scenarios, based on critical numbers of K obtained in sensitivity tests, below which the population would be unviable. Our PVAs suggests that hunting has a higher impact on population viability in comparison to threats from the pet trade. Annual losses of adult and young females from hunting had the most detrimental effect on population persistence under all forest fragment sizes. Such hunting pressure is not sustainable for populations living in areas ≤3,460 ha, since these areas may not support populations of ≥84 individuals. The seven largest of the 13 protected areas currently harboring capuchins should be effective at maintaining viable populations in the long term even under the greatest threat scenarios we modeled. Other large forest patches, mainly in the western part of the species distribution, are recommended as priority areas for protection to increase the chances of capuchins' survival for the long term. In addition, forest fragments of ≤782.8 ha cannot maintain viable populations, even when there are no threats from hunting or from captures for the pet trade. Increased law enforcement is necessary to prevent the hunting and capture of capuchins, especially within larger forest fragments. Am. J. Primatol. 78:950-960, 2016. © 2016 Wiley Periodicals, Inc.

Survey of Plasmodium in the golden-headed lion tamarin (Leontopithecus chrysomelas) living in urban Atlantic forest in Rio de Janeiro, Brazil.

BACKGROUND: Communicating the presence of potential zoonotic pathogens such as Plasmodium spp. in wild animals is important for developing both animal and human health policies. METHODS: The translocation of an exotic and invasive population of Leontopithecus chrysomelas (golden-headed lion tamarins) required the screening of these animals for specific pathogens. This studies objective was to investigate Plasmodium spp. infection in the L. chrysomelas, both to know its prevalence in these animals in the local area and to minimize the risk of pathogens being translocated to the destination site. To investigate Plasmodium spp. infection, blood samples from 268 animals were assessed for the presence of Plasmodium spp. by genus-specific PCR and stained thick and thin blood smears were examined by light microscopy. Data of human malaria infection in the studied region was also assembled from SINAN (Diseases Information System Notification-Ministry of Health of Brazil). RESULTS: Results from the PCR and microscopy were all negative and suggested that no L. chrysomelas was infected with Plasmodium spp. Analysis of SINAN data showed that malaria transmission is present among the human population in the studied region. CONCLUSIONS: This study is the first to provide information on Plasmodium spp. infection in L. chrysomelas. Plasmodium spp. infection of this species is rare or absent though malaria parasites circulate in the region. In addition, there is minimal risk of translocating Plasmodium spp. infected animals to the destination site.

Pervasive defaunation of forest remnants in a tropical biodiversity hotspot.

Tropical deforestation and forest fragmentation are among the most important biodiversity conservation issues worldwide, yet local extinctions of millions of animal and plant populations stranded in unprotected forest remnants remain poorly explained. Here, we report unprecedented rates of local extinctions of medium to large-bodied mammals in one of the world's most important tropical biodiversity hotspots. We scrutinized 8,846 person-years of local knowledge to derive patch occupancy data for 18 mammal species within 196 forest patches across a 252,669-km(2) study region of the Brazilian Atlantic Forest. We uncovered a staggering rate of local extinctions in the mammal fauna, with only 767 from a possible 3,528 populations still persisting. On average, forest patches retained 3.9 out of 18 potential species occupancies, and geographic ranges had contracted to 0-14.4% of their former distributions, including five large-bodied species that had been extirpated at a regional scale. Forest fragments were highly accessible to hunters and exposed to edge effects and fires, thereby severely diminishing the predictive power of species-area relationships, with the power model explaining only ~9% of the variation in species richness per patch. Hence, conventional species-area curves provided over-optimistic estimates of species persistence in that most forest fragments had lost species at a much faster rate than predicted by habitat loss alone.

First record of tool use by wild populations of the yellow-breasted capuchin monkey (Cebus xanthosternos) and new records for the bearded capuchin (Cebus libidinosus).

Reports on use of stones as hammers and anvils to open hard nuts by wild capuchin monkeys are scarce and limited to Cebus libidinosus. Here, we report for the first time data on tool use-stones as hammer and anvils to open nuts-in wild C. xanthosternos and a description of new tool using sites for C. libidinosus. Our records were made by visiting anvil sites and by information obtained from local residents. We surveyed three different biomes: Caatinga (dry forest and thorn scrub), Cerrado (Brazilian bush savannah), and Atlantic forest (wet forest), all records of tool use were from Caatinga or transitional areas between habitats. The behavior is suggested to be routinely performed and widespread among several populations. The fruits of six plant species in different localities were opened with hammer stones by C. xanthosternos. Hammer stones were of similar weigh as those described in other studies of C. libidinosus. Conditions found in Caatinga, such as a more frequent use of the ground by the monkeys and/or food scarcity, may play an important role in the acquisition of nut-cracking behavior. The absence of more reports of nut cracking and other forms of tool use in other species of wild Cebus is likely to result from a lack of surveys in very dry and food-limited habitats or intrinsic characteristics of other Cebus species.