A New Assessment of Robust Capuchin Monkey (Sapajus) Evolutionary History Using Genome-Wide SNP Marker Data and a Bayesian Approach to Species Delimitation.

Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey.

No Evidence of Rabies Exposure in Wild Marmosets (Callithrix jacchus) of Northeast Brazil.

Rabies transmitted by wildlife is the main source of human rabies mortality in Latin America and considered an emerging disease. The common marmoset Callithrix jacchus of Brazil is the only known primate reservoir of rabies worldwide. We tested whether alive free-ranging C. jacchus were exposed to rabies in four northeast states that have previously reported rabies-positive dead C. jacchus (Pernambuco and Bahia) or not (Paraíba and Rio Grande do Norte). Our results show no evidence of rabies antibodies or infection in the sampled C. jacchus, suggesting that apparently healthy marmosets are not widely exposed to rabies over their natural range.

A green racer snake (Philodryas nattereri, Colubridae) killed but not eaten by a blonde capuchin monkey (Sapajus flavius, Cebidae).

We report the killing of a snake (Philodryas nattereri, Colubridae) by a blonde capuchin monkey (Sapajus flavius, Cebidae). This endemic primate species from the northeast of Brazil includes vertebrates such as lizards and marsupials in its diet, but we can find no previously published record of an attack upon or consumption of snakes by this species of platyrhine monkey. During the attack, the group mobbed the snake, with individuals uttering agonistic vocalizations and displaying behaviors such as raising their tails, moving tree branches, piloerecting, and baring their teeth. An adult male monkey seized the snake, bit and twisted its body, thereby killing it; he then dropped the carcass onto tree branches, but did not consume it. This single event suggests that this Cebidae species may be able to distinguish dangerous from harmless snakes, and it also may be an example of a lethally violent reaction to a potential predator or competitor, exemplifying the plasticity and cognitive skills exhibited by genus Sapajus.

Limited Evidence for Infection of Urban and Peri-urban Nonhuman Primates with Zika and Chikungunya Viruses in Brazil.

Chikungunya virus (CHIKV) and Zika virus (ZIKV) emerged in the Americas in 2013. Limited antigenic variability of CHIKV and ZIKV may restrict urban transmission cycles due to population protective immunity. In Africa, sylvatic transmission cycles involving nonhuman primates (NHP) are known for CHIKV and ZIKV, causing cyclic reemergence in humans. To evaluate whether sylvatic cycles can be expected in Latin America, we tested 207 NHP collected between 2012 and 2017 in urban and peri-urban settings in Brazil for infection with ZIKV and CHIKV. No animal tested positive for viral RNA in genus-specific and species-specific reverse transcription-PCR (RT-PCR) assays. In contrast, six animals (2.9%) from the families Atelidae, Callitrichidae, and Cebidae showed ZIKV-specific antibodies and 11 (5.3%) showed CHIKV-specific antibodies in plaque reduction neutralization tests (PRNT). Reactivity was monotypic against either ZIKV or CHIKV in all cases, opposing unspecific virucidal activity of sera. PRNT endpoint titers were low at 1:40 in all NHP, and positive specimens did not correspond to the likely dispersal route and time of introduction of both arboviruses. All antibody-positive samples were therefore tested against the NHP-associated yellow fever virus (YFV) and Mayaro virus (MAYV) and against the human-associated dengue virus (DENV) by PRNT. Two ZIKV-positive samples were simultaneously DENV positive and two CHIKV-positive samples were simultaneously MAYV positive, at titers of 1:40 to 1:160. This suggested cross-reactive antibodies against heterologous alphaviruses and flaviviruses in 24% of ZIKV-positive/CHIKV-positive sera. In sum, low seroprevalence, invariably low antibody titers, and the distribution of positive specimens call into question the capability of ZIKV and CHIKV to infect New World NHP and establish sylvatic transmission cycles. IMPORTANCE Since 2013, Zika virus (ZIKV) and chikungunya virus (CHIKV) have infected millions of people in the Americas via urban transmission cycles. Nonhuman primates (NHP) are involved in sylvatic transmission cycles maintaining ZIKV and CHIKV in the Old World. We tested NHP sampled during 2012 to 2017 in urban and peri-urban areas severely affected by ZIKV and CHIKV in Brazil. Seroprevalence and antibody titers were low for both viruses. Additionally, we found evidence for infection by heterologous viruses eliciting cross-reactive antibodies. Our data suggest that urban or peri-urban NHP are not easily infected by ZIKV and CHIKV despite intense local transmission. These data may imply that the ZIKV and CHIKV outbreaks in the Americas cannot be sustained in urban or peri-urban NHP once human population immunity limits urban transmission cycles. Investigation of diverse animals is urgently required to determine the fate of the ZIKV and CHIKV outbreaks in the Americas.

Local Ecological Knowledge about Endangered Primates in a Rural Community in Paraíba, Brazil.

The study of local ecological knowledge (LEK) fosters a better understanding of the relationship between humans and the environment. We assessed respondents' ecological knowledge of primates in a rural community located near the Atlantic Forest remnants in the state of Paraíba, Brazil. Populations of Alouatta belzebul (red-handed howler monkeys), Sapajus flavius (blonde capuchins), and Callithrix jacchus (the common marmoset) inhabit the region. We conducted 200 semi-structured interviews and applied thematic content analysis, with weighting, to the responses to quantify the LEK. Respondents showed a low LEK, despite the community's proximity to forest remnants. However, the LEK was significantly higher among men, as well as among those who had a greater degree of contact with the primates. Age did not influence LEK. The studied community apparently does not intensively exploit the forest resources nor does it economically depend on primates, which may explain these individuals' low levels of knowledge about these animals. Such data may support future studies, as well as environmental education and action plans, especially for A. belzebul and S. flavius, both of which are endangered species and targets of the National Action Plan for the Conservation of the Primates of the Northeast.