Parasites and Viruses in Callithrix in Brazil.

PURPOSE: As a result of environmental imbalances of anthropogenic origin, the potential for transmission of parasites and viruses between different primates, including humans, might increase. Thus, parasitic studies have great relevance to primatology, which motivated us to conduct a literature review to synthesize the information available in American primates of the Callithrix genus. METHODS: We carried out the bibliographic search on the main groups of parasites (protozoa, helminths, arthropods, ectoparasites) and viruses found in Callithrix in Brazil in search platforms and consider all manuscript that appeared in search engines, published between the years 1910 and December 2022. In each selected article, the following information was recorded: the host species; parasite taxa; scientific classification of the parasite; host habitat (free-living, captive); diagnostic technique; state; and bibliographic reference. Data were tabulated and arranged in a parasite-host table. RESULTS: Some endemic genera, such as Callithrix, are widely distributed geographically across Brazil and have characteristics of adaptation to different habitats due to their flexibility in diet and behavior. These factors can make them subject to a greater diversity of parasites and viruses in the country. Here, we identified 68 parasitic taxa, belonging to the clades protozoa (n = 22), helminths (n = 34), ectoparasites (n = 7), and viruses (n = 5). Out of this total, 19 have zoonotic potential. Of the six existing marmoset species, Callithrix jacchus was the most frequent in studies, and Callithrix flaviceps did not have reports. All regions of the country had occurrences, mainly the Southeast, where 54% of the cases were reported. In 46% of the reported parasites and viruses, it was not possible to identify the corresponding species. CONCLUSION: We conclude that in part of the works the identification methods are not being specific, which makes it difficult to identify the species that affects Callithrix spp. Furthermore, the studies present geographic disparities, being concentrated in the southeast of the country, making it impossible to have a more uniform analysis of the findings. Thus, it is observed that information about parasites and viruses is incipient in the genus Callithrix in Brazil.

Climate change effects on the distribution of yellow-breasted capuchin monkey (Sapajus xanthosternos (Wied-Neuwied, 1826)).

The magnitude of recent climatic changes has no historical precedent and impacts biodiversity. Climatic changes may displace suitable habitats (areas with suitable climates), leading to global biodiversity decline. Primates are among the most affected groups. Most primates depend on forests and contribute to their maintenance. We evaluated the potential effects of climatic change on the distribution of Sapajus xanthosternos, a critically endangered primate whose geographical range encompasses three Brazilian biomes. We evaluated changes between baseline (1970-2000) and future (2081-2100) climates using multivariate analysis. Then, we compared current and future (2100) climatic suitability projections for the species. The climatic changes predicted throughout the S. xanthosternos range differed mostly longitudinally, with higher temperature increases in the west and higher precipitation reductions in the east. Climatic suitability for S. xanthosternos is predicted to decline in the future. Areas with highest current climatic suitability occur as a narrow strip in the eastern part of the geographic range throughout the latitudinal range. In the future, areas with highest values are projected to be located as an even narrower strip in the eastern part of the geographical range. A small portion of forest remnants larger than 150 ha located in the east has larger current and future suitability values. At this large scale, the spatial heterogeneity of the climate effects reinforce the importance of maintenance of current populations in different areas of the range. The possibility that phenotypic plasticity helps primates cope with reduced climatic suitability may be mediated by habitat availability, quality, and connectivity.

Gastrointestinal parasites in free-ranging common marmosets (Callithrix jacchus Linnaeus, 1758) in the state of Sergipe, northeastern Brazil.

Ecological interactions resulting from human interference and environmental changes have implications for human health and the host animals involved in the parasite cycles. Considering the scarcity of surveys of the parasitic fauna of non-human primates in northeastern Brazil, the objective of this study was to investigate the infection by gastrointestinal parasites in free-ranging common marmosets (Callithrix jacchus) in the State of Sergipe. Fecal samples were collected from 52 animals captured in three protected areas. Most of the samples consisted of adult females and 57% were infected with at least one of the 12 identified parasite taxa. The most frequent intestinal parasite was Prosthenorchis sp., followed by Spiruridae, Entamoeba spp. and Strongylida order. The presence of gastrointestinal parasites was not dependent on sex, age or weight, although there was an association with the capture biome.

Primates facing climate crisis in a tropical forest hotspot will lose climatic suitable geographical range.

Global climate changes affect biodiversity and cause species distribution shifts, contractions, and expansions. Climate change and disease are emerging threats to primates, and approximately one-quarter of primates' ranges have temperatures over historical ones. How will climate changes influence Atlantic Forest primate ranges? We used habitat suitability models and measured potential changes in area and distributions shifts. Climate change expected in 2100 may change the distribution area of Atlantic Forest primates. Fourteen species (74%) are predicted to lose more than 50% of their distribution, and nine species (47%) are predicted to lose more than 75% of their distribution. The balance was negative, indicating a potential future loss, and the strength of the reduction in the distribution is related to the severity of climate change (SSP scenarios). Directional shifts were detected to the south. The projected mean centroid latitudinal shift is ~ 51 km to the south for 2100 SSP5-8.5 scenario. The possibility of dispersal will depend on suitable routes and landscape configuration. Greenhouse gas emissions should be urgently reduced. Our results also emphasize that no more forest loss is acceptable in Atlantic Forest, and restoration, canopy bridges, friendly agroecosystems, and monitoring of infrastructure projects are urgent to enable dealing with climate change.

Temperature and exudativory as drivers of the marmoset (Callithrix spp.) daily activity period.

Primates are affected by fluctuations in ambient temperatures, mostly through thermoregulatory costs and changes in the availability of food. In the present study, we investigate whether the ambient temperature and proxies of food availability affect the activity period of marmosets (Callithrix spp.). We predicted that: (i) at colder sites, marmosets would spend more time at sleeping sites; (ii) midday resting bouts would be longer at hotter sites; (iii) the onset/cessation of activity and resting behavior at midday would be more closely related to temperature than food availability, and (iv) highly exudativorous groups would have higher total levels of resting. We compiled data on the onset and cessation of activity and the time spent resting at midday from seven marmoset studies from sites with a wide range of temperatures. We used generalized linear mixed models to verify the relationship between the dependent variables (lag between dawn and the onset of activities, lag between cessation of activities and dusk, and proportion of resting during midday) and the minimum and maximum temperatures at the respective study sites, together with proxies of food availability (exudativory rates, the amount of habitat available per individual, and net primary productivity) using each sample month as a sampling unit and the identity of the study as a categorical random factor. At colder sites and during colder months, the marmosets left sleeping trees later in the morning and ceased their activities earlier, while at hotter sites and during hotter months, they spent more time resting during midday. More exudativorous groups become active later in the morning, but also ceased their activities later. The abundance of food did not affect the timing of activities. We provide evidence that both low and high temperatures affect marmosets' activities, and that their activity period appears to be more influenced by the thermal environment than food availability.

Non-volant mammals of the Ibura National Forest, northeastern Brazil

Less than 10% of the original Atlantic Forest cover now remains standing in the Brazilian state of Sergipe, although few scientific studies have focused on its mammalian diversity. The present study describes the diversity of non-volant mammals found in the Ibura National Forest (INF), based on live trapping, and direct and indirect observations. We sampled the IBF on six days per month between June 2012 and August 2013, using live-traps (Sherman-type) positioned in pairs (ground and understory). We equally sampled semideciduous forest and an abandoned Eucalyptusplantation with dense understory (over 30 years). We also used non-systematics methods (direct observations, vestiges, camera-trap, and opportunistic captures). We recorded 18 species, from 12 families and 7 orders considering all the applied methods. Among recorded species, Bradypus torquatusand Lontra longicaudisare considered threatened of extinction. Considering only the live-trapping (totaling 3,240 trapping nights), we captured 125 individuals (3.85% success) from four species, Marmosa demerarae(52%), Didelphis albiventris(19.2%), Cerradomys vivoi(15.2%), and M. murina(13.6%). Estimated and observed richness was the same, suggesting a satisfactory effort. Didelphis albiventrisand M. demeraraeshowed significantly higher captures in the dry seasons. Didelphis albiventrisand C.vivoishowed significantly higher captures in the substratum, and M. demeraraehigher in the understory. Cerradomysvivoishowed significantly higher captures in the Eucalyptusphytophysiognomy. Non-Metric Multidimensional Scaling and the ANOSIM showed a significant difference in the captured species among semidecidual forest and Eucalyptus. Despite the small area (144 ha), the INF still houses a relatively high mammalian diversity. Further investigations may help to understand the role of habitat reduction in the diversity and habitat partitioning among mammal species in the Atlantic Forest of Northeastern Brazil.

Anointing with commercial insect repellent by free-ranging Cebus capucinus in Manuel Antonio National Park, Quepos, Costa Rica.

Fur rubbing or anointing is a well known behavior in capuchin monkeys (Cebus and Sapajus), and may have medicinal and/or social functions. Observations of anointing in capuchins have recorded the application of substances derived from both plants (orange, onion, garlic, citronella, and lemongrass) and animals (ants and millipedes). The present study reports on anointing behavior in free-ranging white-headed capuchins, Cebus capucinus, which involved a commercial insect repellent. After looting a bottle of repellent from the bag of a visitor to the Manuel Antonio National Park in Costa Rica, an adult male bit open the bottle and rubbed the leaking liquid over its entire body, focusing mainly on its belly. Other members of the group rubbed themselves against the male's body and were eventually able to retrieve the bottle of repellent and anoint themselves. The repellent is composed mainly of extracts of eucalyptus and citronella. The capuchins may have been attracted by the strong citric scent of the citronella, which is known to stimulate fur-rubbing behavior in these monkeys. This is reinforced by the fact that the sequence of events was quite distinct from that associated with an earlier event, in which a juvenile male looted, tasted, and then discarded a stick of lip gloss and a tube of sunblock. Overall, the observations indicate that the citric scent of the repellent was attractive to the capuchins, especially in comparison with other man-made substances. As the animals partially ingested all the substances, there is clearly a need for more effective regulation of the contact between animals and visitors in the park.

Survey on helminths and protozoa of free-living Neotropical bats from Northeastern Brazil.

Bats are considered important reservoirs of pathogens of veterinary and medical relevance worldwide. However, despite the increasing attention paid towards the central role of bats in the spreading of some zoonotic infections, studies on their own parasites remain patchy especially in Neotropical regions. Understanding the relationships occurring between bats and their pathogens is a crucial step to determine the implications undermining the ecology and biology of these animals. The present study aims to assess the endoparasitic fauna of Neotropical bats from Northeastern Brazil, with a particular focus on helminths and protozoa. From October 2016 to March 2017, 54 fresh faecal samples were collected in stable shelters inhabited by three different bat species (i.e., Molossus molossus, Myotis lavali and Noctilio albiventris). Samples were analysed using four different techniques (i.e., Centrifugal Sedimentation, Flotation Technique, Spontaneous Sedimentation Technique and FLOTAC®). A total of 96.29% (52/54) samples were positive for at least one gastrointestinal parasite and 11 different families were identified. In particular, 63.6% (7/11) of the families were of helminths and 36.4% (4/11) of protozoa. Helminths were classified into two different classes (Nematoda and Cestoda) and seven families, whereas the four protozoa classes detected (i.e., Coccidia, Gregarinomorphe, Lobosea and Zoomastigophora) into four families. Eggs of Ancylostomatidae and Hymenolepididae were the most abundan. The findings of this present study demonstrate that Neotropical bats from Northeastern Brazil are parasitized by a wide number of parasites, and some of them may have important implications for Public Health.

Self-anointing behaviour in captive titi monkeys (Callicebus spp.).

Self-anointing behaviour using Bauhinia sp. was reported in two captive titi monkeys (Callicebus coimbrai and Callicebus barbarabrownae). The study was carried out from October 2013 to May 2014 during an experimental study investigating the gut passage time of these individuals at the Getúlio Vargas Zoobotanical Park, north-eastern Brazil. Although leaves, petioles and flowers of Bauhinia contain chemical substances that could affect the presence of ectoparasites, it is unclear if titi monkeys demonstrate self-anointing behaviour as a method of self-medication. However, due to the presence of large glands in C. coimbrai and C. barbarabrownae chests, and the high frequency of occurrence observed for the adult male, we cautiously suggest that the use of Bauhinia may be linked to olfactory communication.

A primate at risk in Northeast Brazil: local extinctions of Coimbra Filho's titi (Callicebus coimbrai).

Identifying the factors that determine local extinction of populations is crucial to ensure species conservation. Forest-dwelling primates are especially vulnerable to habitat fragmentation, although few studies have provided systematic evidence of local extinctions. Over an 11-year period, approximately 100 remnant populations of the endangered Coimbra Filho's titi monkey (Callicebus coimbrai) have been found within the geographic range of the species in Bahia and Sergipe, Northeast Brazil. During the present study, extinction of 13 of these populations was recorded through intensive surveys. These extinctions were detected from evidence of intensive logging and clear-cutting, interviews with local residents and systematic searches of the sites where occurrence of the species had been confirmed in previous surveys. These local extinctions represent approximately 10 % of the known populations of C. coimbrai and up to 28.3 % of the area occupied by the species. Comparison of the vegetation structure in fragments where extinction was recorded and where the species still occurs indicated that sparser understorey may be a correlate of extinction, combined with the fact that extinctions occurred within fragments characterised by relatively high levels of anthropogenic disturbance. These findings reinforce the Endangered status of the species and the urgent need for intensification of conservation measures within the most impacted areas of the geographic distribution of C. coimbrai.

Functional planning units for the management of an endangered Brazilian titi monkey.

Conservation practices in the tropics often rely on the data available for a few, better-known species and the adoption of an appropriate spatial scale. By defining a set of landscape units that account for critical aspects of the focal species, the information available on these conservation targets can support regional conservation policies. Here, we define and classify adjacent landscapes, termed planning units, to orientate management decisions within and among these landscapes, which are occupied by an endangered flagship primate species (Coimbra-Filho's titi monkey, Callicebus coimbrai) from eastern Brazil. We use landscape boundaries (highways and river systems), and a high-resolution map of forest remnants to identify continuous and manageable landscapes. We employed functional landscape metrics based on the species' dispersal ability and home range size to characterize and classify these landscapes. We classified planning units by scoring them according to a suite of selected metrics through a Principal Component Analysis. We propose 31 planning units, containing one to six C. coimbrai populations, most with low values of habitat availability, functional connectivity and carrying capacity, and a high degree of degradation. Due to this poor landscape configuration, basic management practices are recommendable. However, additional aspects of the landscapes and the populations they contain (e.g., matrix type and genetic variability) should improve the scheme, which will require a closer integration of research aims with socio-political strategies. Even so, our scheme should prove useful for the combination of information on conservation targets (i.e., focal species) with management strategies on an administrative scale.

Climate and land use changes will degrade the configuration of the landscape for titi monkeys in eastern Brazil.

Land use changes have profound effects on populations of Neotropical primates, and ongoing climate change is expected to aggravate this scenario. The titi monkeys from eastern Brazil (Callicebus personatus group) have been particularly affected by this process, with four of the five species now allocated to threatened conservation status categories. Here, we estimate the changes in the distribution of these titi monkeys caused by changes in both climate and land use. We also use demographic-based, functional landscape metrics to assess the magnitude of the change in landscape conditions for the distribution predicted for each species. We built species distribution models (SDMs) based on maximum entropy for current and future conditions (2070), allowing for different global circulation models and contrasting scenarios of glasshouse gas concentrations. We refined the SDMs using a high-resolution map of habitat remnants. We then calculated habitat availability and connectivity based on home-range size and the dispersal limitations of the individual, in the context of a predicted loss of 10% of forest cover in the future. The landscape configuration is predicted to be degraded for all species, regardless of the climatic settings. This include reductions in the total cover of forest remnants, patch size and functional connectivity. As the landscape configuration should deteriorate severely in the future for all species, the prevention of further loss of populations will only be achieved through habitat restoration and reconnection to counteract the negative effects for these and several other co-occurring species.

Forest structure drives global diversity of primates.

Geographic gradients in the species richness of non-human primates have traditionally been attributed to the variation in forest productivity (related to precipitation levels), although an all-inclusive, global-scale analysis has never been conducted. We perform a more comprehensive test on the role of precipitation and biomass production and propose an alternative hypothesis - the variation in vertical structure of forest habitats as measured by forest canopy height - in determining primate species richness on a global scale. Considering the potential causal relationships among precipitation, productivity and forest structure, we arranged these variables within a path framework to assess their direct and indirect associations with the pattern of primate species richness using structural equation modelling. The analysis also accounted for the influence of spatial autocorrelation in the relationships and assessed possible historical differences among biogeographical regions. The path coefficients indicate that forest canopy height (used as a proxy for vertical forest structure) is a better predictor of primate species richness than either precipitation or productivity on both global and continental scales. The only exception was Asia, where precipitation prevailed, albeit independently from productivity or forest structure. The influence of spatially structured processes varied markedly among biogeographical regions. Our results challenge the traditional rainfall-based viewpoint in favour of forest distribution and structure as primary drivers of primate species richness, which aggregate potential effects from both climatic factors and habitat complexity. These findings may support predictions of the impact of forest removal on primate species richness.

Use of alternative plant resources by common marmosets (Callithrix jacchus) in the semi-arid caatinga scrub forests of northeastern Brazil.

The common marmoset (Callithrix jacchus) is amply distributed in the Brazilian Northeast, but little is known of its ecology in the semi-arid Caatinga scrublands. The present study provides the first detailed data on the composition of the diet of C. jacchus in Caatinga ecosystems, derived from observations at four sites in the state of Sergipe. While exudate sources were gouged at all four sites in a manner typical of the species, fruit was the principal component of the diet at the main study site during most months, and a number of unusual items were eaten, including leaves, and the reproductive parts of cacti and bromeliads. These plants are rarely recorded in marmoset diets, but are common in caatinga habitats. Leaves were ingested during 5 of the 8 months monitored at the main study site, reaching 39.74% of the diet in 1 month, and appeared to be an alternative fallback food to plant exudates during periods when fruit was scarce. Three species of cactus provided both flowers and fruits, while the terrestrial bromeliad, Encholirium spectabile, provided nectar (30.81% of the diet in November). Approximately half of the plant species (and three families) identified in this study had not been recorded previously in the diet of Callithrix. Overall, the data suggest that, while the marmosets exploit the same types of plant foods in the Caatinga, the resource base is quite distinct from that of the Atlantic Forest. Other differences, such as relatively small groups and large home ranges, may contribute to divergent ecological patterns, which require more systematic investigation. Am. J. Primatol. 75:333-341, 2013. © 2012 Wiley Periodicals, Inc.

Do snakes represent the principal predatory threat to callitrichids? Fatal attack of a viper (Bothrops leucurus) on a common marmoset (Callithrix jacchus) in the Atlantic Forest of the Brazilian Northeast.

A juvenile common marmoset (Callithrix jacchus) was attacked by a whitetail lancehead viper (Bothrops leucurus) while playing with other group members close to the ground at a site in northeastern Brazil. The attack was almost immediately fatal, but the viper was unable to ingest the body of the marmoset. After approximately 10 min, during which it attempted to swallow the marmoset a number of times, the viper moved away, abandoning the body. While raptors are the principal predators of callitrichids, this record reinforces the relative vulnerability of these primates to snakes in comparison with other platyrrhines, although the small number of recorded events precludes a more definitive analysis of the phenomenon.

Birds of the Grota do Angico Natural Monument in the semi-arid Caatinga scrublands of northeastern Brazil / Aves do Monumento Natural Grota de Angico na região de Caatinga ao Nordeste do Brasil

An inventory of the avian fauna of the Grota do Angico Natural Monument in the Caatinga of northern Sergipe, Brazil, revealed the presence of at least 140 species, including nine that are endemic to the Caatinga and seasonal forest adjacent. Despite the limited scope of the study (two expeditions in July and August, 2008), the species richness recorded at the site appeared to be typical of the region and the Caatinga biome.

No inventário da avifauna do Monumento Natural Grota de Angico na Caatinga ao norte de Sergipe, Brasil, revelou a presença de pelo menos 140 espécies, incluindo nove endêmicas da Caatinga e florestas sazonais adjacentes. Apesar do alcance limitado do estudo (duas expedições em Julho e Agosto, 2008), a riqueza de espécies registrada no sitio aparentemente pode ser típica da região e do Bioma Caatinga.