Diet and seed dispersal of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park.

The dietary ecology of a species can provide information on habitat requirements, food resources, and trophic interactions, important to guide conservation efforts of wildlife populations in endangered habitats. In this study, we investigated the dietary ecology of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park, in the endangered Cerrado biome of central Brazil. To obtain diet composition and evaluate the role of these primates as seed dispersers of local tree species, fecal sample collections and feeding observations were performed for a 7-month period. To determine whether seeds germinated better after passing through a primate gut, we conducted germination trials with (i) pulped seeds from trees, (ii) depulped seeds from trees, (iii) seeds from feces planted with feces, and (iv) seeds from feces planted without feces. During experimental procedures, 7308 seeds from 8 families and 10 species were planted. We found that S. libidinosus spent more time feeding on fruits than on any other food item and the diet consisted of 33 plant species from 21 families. However, 20% of their diet consisted of anthropic food. Most seeds planted with feces germinated faster compared to seeds in other experimental treatments, suggesting that passing through the gut and being deposited with fecal material is advantageous. The bearded capuchins also defecated many medium- (5 species) and large-sized (2 species) seeds that may be inaccessible to smaller arboreal frugivores. The results obtained emphasize the important role of bearded capuchins as seed dispersers for the maintenance and conservation of the endangered Cerrado biome.

A new addition to the toolbox: stone tool use in blonde capuchin monkeys (Sapajus flavius).

The use of tools played a central role in human culture and evolution. Early studies with apes demonstrated the tool use; however, currently the works have focused on Platyrrhine, particularly capuchin monkeys. Blonde capuchin monkeys, Sapajus flavius, have been observed using sticks to fish for termites in the Atlantic Forest, where this species has been extensively studied. In this study, we presented the first evidence of stone tool use by the blonde capuchin monkeys, as well as the dimensions and weight of these tools. We gathered data from three areas of Caatinga dry forest where we discovered this new tool use among the species. The mean weight of the hammers was 475.7 g (± 142 SD). The mean height of the anvils was 48.3 cm (± 18.7 SD), while the mean surface area of the anvils was 1.2 m2 (± 0.4 SD). We identified fruits and/or nuts from three plant species-Prunus dulces, Cnidoscolus quercifolius, and Syagrus coronate-near the anvils at the study sites. Additionally, we passively observed six instances of stone tool use by blonde capuchin monkeys. Their use of stones to crack encased foods mirrored behaviors previously reported in Sapajus libidinosus, a species well known for using stone tools to exploit hard nuts. Our findings place blonde capuchin monkeys among the list of primates that utilize stones as tools, highlighting the species' adaptability in exploiting resources within the Caatinga. Long-term studies are essentials to comprehend the use pattern of stone tools (across both general and seasonal perspectives) and the influence of variables, such as fruit hardness, distance to watercourses, and fruit availability on the use of this technology by this primate.

Direct links between resource availability and activity budget better reveal ecological patterns of endangered Coimbra-Filho's titi monkey.

Many primatological studies do not assess direct indexes of food availability to make inferences about behavioral strategies. We related the diet and behavior of a group of Callicebus coimbrai in northeastern Brazil to fruit availability indexes and compared this pattern between seasons (direct and indirect assessment of food availability) to assess whether direct and indirect approaches detect similar ecological patterns. We monitored the study group for 33 months (5 days/month) via scan sampling. The monthly availability of fruits and new leaves was recorded in phenological transects. Fruit availability varied across years based on fruit prevalence, and timing and duration of the abundant seasons. We did not find evidence of a time-minimizing strategy, since C. coimbrai did not change its activity levels according to food availability. However, the negative relationship between foraging and fruit availability indicates that C. coimbrai can compensate for the lower fruit availability by increasing the search for alternative food sources. Monthly fruit consumption was positively correlated to fruit availability and negatively related to the consumption of other food items. However, the behavioral and feeding profiles did not vary between seasons and were not related to rainfall levels. Primate studies should directly relate behavioral and feeding profiles to fruit availability indices, thus avoiding using seasons as proxies of food availability.

Microsatellite Markers for Bearded Capuchins (Sapajus libidinosus): Transferability and Characterization.

Natural Sapajus libidinosus populations are in continuous decline due to fragmentation, habitat loss, and the illegal pet trade. They live in Caatinga scrub forests, which already lost over 50% of their original cover. The lack of studies on S. libidinosus population genetics means that we do not know how they are being affected by this striking habitat loss and other anthropogenic disturbances. Polymorphic markers are not available for the study of S. libidinosus diversity and population genetics. Thus, here we aimed to test the transferability of 14 microsatellite markers to S. libidinosus. These microsatellites were previously isolated from Cebus capucinus (white-faced capuchin), species belonging to the same subfamily (Cebinae) as the study species. We found that six of the tested microsatellite markers (tetra-nucleotide) were cross-amplified in our target species. All loci were polymorphic. The number of alleles varied from 4 to 7, and the expected heterozygosity ranged from 0.588 to 0.869. The microsatellite markers transferred to S. libidinosus and characterised in our study will be valuable tools to evaluate the genetic variability of both wild and captive populations. They will considerably reduce the costs of microsatellite isolations, helping to prioritise currently limited research and conservation budgets in Brazil.

For emergency only: terrestrial feeding in Coimbra-Filho's titis reflects seasonal arboreal resource availability.

Terrestriality in Platyrrhine primates is primarily associated with low arboreal resource availability, low predation risk when on the ground and increased contact time with human observers. To test the relationship between these variables and ground use frequency, we studied a group of endangered Coimbra-Filho's titi monkeys (Callicebus coimbrai) in a 14-ha forest fragment in north-eastern Brazil. Terrestriality data were collected on a monthly basis (33 months) using scan sampling procedures from July 2008 to July 2012. Overall, Coimbra-Filho's titi monkeys were recorded during 0.6% of observation time (113 out of 18,164 scans) on the ground. Most of the time on the ground was spent feeding on young leaves (71 records) and the least amount of time on fruits (14 records). Availability of arboreal foods, rainfall, and time of contact with human observers did not influence overall terrestrial behaviour (ground use). However, the timing and nature of the monkeys' terrestrial feeding was strongly related to the absence of arboreal fruit (ß-estimate = -3.078) and young leaf (ß-estimate = -3.515) food resources. We suggest that terrestrial feeding by Coimbra-Filho's titi monkeys could be an adaptation to low arboreal fruit availability and the exploitation of alternative food resources.

Potential self-medication by brown titi monkeys, Plecturocebus brunneus, in an urban fragment forest in the Brazilian Amazon.

In this study, we report fur-rubbing behavior of brown titi monkeys, Plecturocebus brunneus, using chewed leaves from (Fabaceae) and Piper tuberculatum (Piperaceae). These reports were obtained during systematic monitoring of titi monkeys from May until December 2019 (218 h) in an urban fragment forest in the Brazilian Amazon. Both plant species contain chemical substances in their leaves that potentially repel ectoparasites. The genus Piper is known for its repelling action due to the presence of amides, alkaloids and benzoic acid. The presence of dogs, cats and human settlements may contribute to an increase of ectoparasites, making a potential self-medication function of fur rubbing in this primate species plausible.

Should I store, or should I sync? The breeding strategy of two small Neotropical primates under predictable resource availability.

Primates employ many strategies to deal with the costs of reproduction. While income breeders exploit the food available in their environment during lactation, the most costly phase of reproduction, capital breeders tend to store energy for use in the period. We analyzed the relationship between resource availability and lactation in Callicebus coimbrai (n = 2 groups) and Callicebus nigrifrons (n = 2 groups) in four Brazilian Atlantic forest remnants, to assess their breeding strategy. We recorded the occurrence of births and breastfeeding events to assess birth seasonality and lactation period and length while monitoring monthly fruit availability. We recorded 11 births (five for C. coimbrai, and six for C. nigrifrons), all restricted to the end of the lean season and the beginning of the rich season. Lactation coincided with periods of increased fruit availability. We suggest that the breeding pattern of Callicebus coimbrai and C. nigrifrons is compatible with an income-based breeding strategy.

Can a Non-Native Primate Be a Potential Seed Disperser? A Case Study on Saimiri sciureus in Pernambuco State, Brazil.

The interaction between native fleshy-fruit plants and introduced fruit consumers contributes to the dynamics of highly fragmented environments. Such interactions can occur through pollination and seed dispersal. Here, we investigated the potential of seed dispersing by a non-native primate, the squirrel monkey (Saimiri sciureus), in an urban Atlantic forest fragment in north-eastern Brazil. Fleshy fruits from non-native plants were preferentially exploited by the squirrel monkeys. We measured 147 seeds (width and length) from 20 of 106 faecal samples. The dispersed seeds were from five plant species (four families). We found a positive correlation between the size of seeds found in faecal samples with their availability in the habitat. Only one seed was found visually damaged after passage through the squirrel monkeys' guts. The defecated seeds were uniformly distributed (variance to mean ratio index) in the home range of squirrel monkeys, and there was a lack of specific latrines (i.e., habitat preference for defecation). Our data provide evidence that non-native S. sciureus may in be (i) acting as a potential seed disperser of native plants in the Atlantic forest fragment, (ii) contributing to the ecological role of native frugivores, and (iii) potentially contributing to the regeneration process of the highly degraded study site.

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.

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.

Seasonal versatility in the feeding ecology of a group of titis (Callicebus coimbrai) in the northern Brazilian Atlantic Forest.

The feeding behavior of a group of titis (Callicebus coimbrai) was monitored over an annual cycle at a site in northeastern Brazil. Behavioral data were collected in scan samples (1-min scan at 5-min intervals), and complementary data on fruit availability and new leaf cover were collected. Feeding time accounted for 28.9% of daily activity. Fruit was the principal item of the diet (61.2% of records) and the primary category in all months except September, when it was surpassed by leaves. Young leaves were the second most important category (20.0%). The consumption of seeds and insects was prominent in November and December. Fifty-two plant species were exploited, and the Elaeocarpaceae, Myrtaceae, Sapotaceae, and Passifloraceae provided the vast majority (86.0%) of plant feeding records. The phenological record did not provide a good measure of fruit availability, but a strong correlation (r(s) =0.902, P<0.0001, n=12) was found between the consumption of leaves and the exploitation of lianas each month. Lianas accounted for 28.2% of plant feeding records, and predominated between August and December. This suggests that lianas may represent a key factor in the ability of the species to tolerate the intense habitat fragmentation found throughout its geographic range.

Use of sleeping sites by a titi group (Callicebus coimbrai) in the Brazilian Atlantic Forest.

Predation pressure affects most aspects of primate behaviour, and is especially pronounced in the context of the use of sleeping sites, given the vulnerability of the animal at this time. Most small-bodied platyrrhines have highly systematic patterns of sleeping site choice and use. This study analyses the use of sleeping sites by a free-ranging group of titis (Callicebus coimbrai) monitored at a site in Sergipe, Brazil, between July, 2009 and June, 2010. When the subjects approached a sleeping tree their behaviour was typically cautious, including slow and silent movement, early retirement (20-162 min before sunset on 52 dry afternoons), and sleeping in a tight huddle with their tails entwined. Despite this behaviour, which has an obvious anti-predator function, the group slept in only three different trees during the course of the study, and returned to the same tree used on the previous night on a quarter of evenings (n = 56). This was despite the availability within the group's home range of a large number of trees with similar structural characteristics (i.e. tall, open crown in the upper canopy). Surprisingly, the three trees were all members of the same species, Licania littoralis (Chrysobalanaceae). The choice of this species, which was not an important source of dietary resources, and the repeated use of a small number of sites, did not seem to be related to factors such as ranging or foraging patterns, but may have a been a response to the specific threat from capuchins, Cebus xanthosternos.

Line transect surveying of arboreal monkeys: problems of group size and spread in a highly fragmented landscape.

Line transect surveying is a relatively rapid and efficient procedure for the assessment of primate populations; although the reliability of the resulting density estimates is affected by a number of factors, including habitat configuration. In this study, primate populations were surveyed at a highly fragmented site in northeastern Brazil, where the resident species include the endangered Coimbra-Filho's titi, Callicebus coimbrai, and the critically endangered yellow-breasted capuchin, Cebus xanthosternos. In addition to standard line transect surveys, data were collected on the composition and distribution of resident groups during playback surveys and ecological monitoring. During surveys, a 5.3-km trail system was walked regularly over a 7-month period, accumulating a total transect length of 476 km and 104 sightings of Callicebus and 41 of Cebus (as well as 19 records of a third primate, Callithrix jacchus). Data were analyzed using the DISTANCE program and the Kelker method, using the perpendicular distances to first animal sighted. Estimates of group density were highly discrepant from known values for both species; although in the case of Cebus, this seemed to reflect grouping patterns at the site. For Callicebus, population density was overestimated considerably when known group counts were used. Overall, there seems to be a need for a much more rigorous standardization of procedures, and the analysis and presentation of results, in order to guarantee the most reliable interpretation possible of the data. These considerations are especially important in the case of endangered species, such as those studied here.

Aspectos comparativos das comunidades de aranhas (Araneae) em dois remanescentes de Mata Atlântica do Estado da Bahia, Brasil / x

A Mata Atlântica vem sofrendo um acelerado processo de fragmentação, o que está afetando sua biodiversidade. O objetivo do trabalho foi inventariar as comunidades de aranhas em dois remanescentes de Mata Atlântica do Estado da Bahia, permitindo uma comparação entre a abundância, riqueza e diversidade de espécies entre estas áreas, visando fornecer subsídios para estudos da dinâmica de fragmentos florestais. Foram amostrados remanescentes com tamanhos bastante distintos, o Parque Metropolitano de Pituaçu - Salvador (PMP) com 425 ha e o Parque Municipal da Matinha - Itapetinga (PMM) com nove ha. As aranhas foram capturadas por coleta manual noturna, num transecto de trinta por cinco metros durante uma hora, com esforço total de 10h. Foi coletado um total de 362 indivíduos, distribuídos em 20 famílias, com 152 adultos e 60 espécies, sendo 37 spp. e 12 famílias no PMP e 30 spp. e 16 famílias no PMM. Ao comparar a abundância das famílias mais freqüentes (mínimo de dez capturas) não houve diferenças significativas entre as áreas (U=46,00; p=0,7959), com um índice de similaridade de Sorensen de 82,4 por cento. Quando comparada a riqueza estimada e a abundância de espécies, não houve diferenças significativas entre as duas áreas (U=65.000; p=0,2799) e (U=20755, p=0,1451), respectivamente. Já a diversidade encontrada nas duas áreas, foi maior no PMP (D=8,1922) do que no PMM (D=6,8032). A partir dos resultados, sugere-se que as semelhanças encontradas entre as áreas podem estar relacionadas a fatores ligados aos processos da fragmentação, como histórico de perturbações. Contudo, sugerimos que seja feita uma avaliação a posteriori de outros fatores, como a forma do fragmento, o tipo de vizinhança e efeito de borda, além de outras variáveis, i.e. da composição florística, que possam estar interferindo na dinâmica destes fragmentos e influenciando na comunidade destas aranhas.

The Atlantic Rainforest has suffered a rapid fragmentation process which has directly affected its biodiversity. The aim of the present study was to inventory of the spider community composition in two Atlantic Rainforest remnants in the state of Bahia, in order to enable a comparison of the abundance, richness and species diversity between the plots. The aim is to contribute towards further studies on the dynamics of the forest remnants. The sampled areas were of distinctive sizes, the Pituaçu Metropolitan Park (PMP) in Salvador with 425 hectares and the Matinha City Park (PMM) in Itapetinga with nine hectares. The spiders were collected using the nocturnal manual collection method in a 30m x 5m transect for an hour, totalling 10 hours of sampling effort. A total of 362 individuals were collected, of which 152 were, belonging to 20 families, and 60 species. Of these, 37 species of 12 families were collected in the PMP and 30 species of 16 families in the PMM. The abundance of the most frequent families (minimum of ten captures) did not differ between the plots (U=46,00; p=0.7959), with a Sorensen similarity index of 82,4 percent. Also, the estimates of the abundance and richness do not differ between the areas (U=65.000; p=0.2799 and U=20755, p=0.1451, respectively). Nevertheless, the diversity was higher in the PMP (D=8.1922) than the PMM (D=6.8032). The results suggest that the similarities between the areas may be a consequence of factors related to the fragmentation processes, such as disturbance history. However, other factors, such as the shape of the remnants and the type of neighborhood, apart from other variables, eg. the flora composition, may also interfere on the dynamics of the spider's communities in these fragments.