Mrinalini Watsa

Chronic Plasmodium brasilianum infections in wild Peruvian tamarins

There is an increased interest in potential zoonotic malarias. To date, Plasmodium malariae that infects humans remains indistinguishable from Plasmodium brasilianum, which is widespread among New World primates. Distributed throughout tropical Central and South America, the Callitrichidae are small arboreal primates in which detection of natural Plasmodium infection has been extremely rare. Most prior screening efforts have been limited to small samples, the use of low-probability detection methods, or both. Rarely have screening efforts implemented a longitudinal sampling design. Through an annual mark-recapture program of two sympatric callitrichids, the emperor (Saguinus imperator) and saddleback (Saguinus fuscicollis) tamarins, whole blood samples were screened for Plasmodium by microscopy and nested PCR of the cytochrome b gene across four consecutive years (2012–2015). Following the first field season, approximately 50% of the samples collected each subsequent year were from recaptured individuals. In particular, out of 245 samples from 129 individuals, 11 samples from 6 individuals were positive for Plasmodium, and all but one of these infections was found in S. imperator. Importantly, the cytochrome b sequences were 100% identical to former isolates of P. malariae from humans and P. brasilianum from Saimiri sp. Chronic infections were detected as evidenced by repeated infections (7) from two individuals across the 4-year study period. Furthermore, 4 of the 5 infected emperor tamarins were part of a single group spanning the entire study period. Overall, the low prevalence reported here is consistent with previous findings. This study identifies two new natural hosts for P. brasilianum and provides evidence in support of chronic infections in wildlife populations. Given that callitrichids are often found in mixed-species associations with other primates and can be resilient to human-disturbed environments, they could contribute to the maintenance of P. malariae populations if future work provides entomological and epidemiological evidence indicating human zoonotic infections.

Classification of producer characteristics in primate long calls using neural networks

Primate long calls are high-amplitude vocalizations that can be critical in maintaining intragroup contact and intergroup spacing, and can encode abundant information about a calls producer, such as age, sex, and individual identity. Long calls of the wild emperor (Saguinus imperator) and saddleback (Leontocebus weddelli) tamarins were tested for these identity signals using artificial neural networks, machine-learning models that reduce subjectivity in vocalization classification. To assess whether modelling could be streamlined by using only factors which were responsible for the majority of variation within networks, each series of networks was re-trained after implementing two methods of feature selection. First, networks were trained and run using only the subset of variables whose weights accounted for ≥50% of each original networks variation, as identified by the networks themselves. In the second, only variables implemented by decision trees in predicting outcomes were used. Networks predicted dependent variables above chance (≥58.7% for sex, ≥69.2 for age class, and ≥38.8% for seven to eight individuals), but classification accuracy was not markedly improved by feature selection. Findings are discussed with regard to implications for future studies on identity signaling in vocalizations and streamlining of data analysis.

Temporal and demographic blood parasite dynamics in two free-ranging neotropical primates

Parasite-host relationships are influenced by several factors intrinsic to hosts, such as social standing, group membership, sex, and age. However, in wild populations, temporal variation in parasite distributions and concomitant infections can alter these patterns. We used microscropy and molecular methods to screen for naturally occurring haemoparasitic infections in two Neotropical primate host populations, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, in the lowland tropical rainforests of southeastern Peru. Repeat sampling was conducted from known individuals over a three-year period to test for parasite-host and parasite-parasite associations. Three parasites were detected in L. weddelli including Trypanosoma minasense, Mansonella mariae, and Dipetalonema spp., while S. imperator only hosted the latter two. Temporal variation in prevalence was observed in T. minasense and Dipetalonema spp., confirming the necessity of a multi-year study to evaluate parasite-host relationships in this system. Although callitrichids display a distinct reproductive dominance hierarchy, characterized by single breeding females that typically mate polyandrously and can suppress the reproduction of subdominant females, logistic models did not identify sex or breeding status as determining factors in the presence of these parasites. However, age class had a positive effect on infection with M. mariae and T. minasense, and adults demonstrated higher parasite species richness than juveniles or sub-adults across both species. Body weight had a positive effect on the presence of Dipetalonema spp. The inclusion of co-infection variables in statistical models of parasite presence/absence data improved model fit for two of three parasites. This study verifies the importance and need for broad spectrum and long-term screening of parasite assemblages of natural host populations.

Modeling Developmental Class Provides Insights into Individual Contributions to Infant Survival in Callitrichids

Cooperative breeders live in social groups in which individuals in an age–sex class vary in reproductive development due to reproductive dominance by a few individuals in each group. Among callitrichids, adult males have been implicated in driving group reproductive output, but uneven sampling efforts, the underlying effects of group size, and pseudoreplication at the group and species levels are confounding variables in these analyses. We examined the drivers of group reproductive output in callitrichids by 1) conducting a meta-analysis of published studies of callitrichid group composition; 2) assigning developmental class based on reproductive morphology; and 3) using multivariate modeling to test whether the proportion of individuals of each developmental class predicts the presence and the number of surviving offspring among free-ranging Weddell’s saddleback tamarins (Leontocebus weddelli) and emperor tamarins (Saguinus imperator) in Peru. The meta-analysis revealed that the number of adult females and group size, but not the number of adult males, are significantly correlated with group reproductive output. Statistical models of the new dataset revealed that the proportion of primary breeding males, primary breeding females, and group size predicted whether groups had surviving infants, and that only the proportion of primary breeding females and group size predicted the number of surviving infants. Thus, primary breeding males appear to be necessary for groups to raise any infants, but a higher proportion of primary breeding females and a larger group size increase group reproductive output overall.

All alloparents are not equally valuable: Primary breeders and group size explain group reproductive success in cooperatively breeding primates

Prior research on cooperative breeders has considered correlations between group reproductive output (GRO) and the number of individuals in each age-sex class, but without controlling for uneven sampling efforts, the underlying effects of group size, and pseudoreplication at the group and species levels. Among callitrichids, age-sex classes do not provide meaningful categories, as individuals within an age-sex class can demonstrate varying reproductive development due to reproductive dominance of a few individuals per group. This study re-assesses the drivers of GRO in callitrichids by a) conducting a meta-analysis of published studies of callitrichid group composition; b) determining a novel method to assign developmental class based on reproductive morphology; and c) utilizing a multistep modelling approach to assess whether any sex-based developmental class predicts both the presence and the numbers of surviving offspring among free-ranging saddleback (Leontocebus weddelli) and emperor tamarins (Saguinus imperator) in Peru. The meta-analysis utilizing a historical dataset revealed that adult females and group size, but not the number of adult males is significantly correlated with GRO. Statistical models of the new dataset revealed that only mature males predicted if groups had any infants at all, but that the number of surviving infants was predicted by mature females and group size. Thus mature males appear to be necessary for groups to raise any infants, but mature females and a larger group size increase group reproductive output overall.The effect of a cooperatively breeding group′s composition on its reproductive output (GRO) has been difficult to assess across populations and species. Prior research has correlated GRO with age and sex classes, not accounting for uneven sample sizes and pseudoreplication at the group or species level. This study utilizes a multistep modelling approach to assess whether breeding status explains GRO better than age-sex classes among free-ranging saddleback ( Saguinus weddelli ) and emperor tamarins ( S. imperator ) in Peru. Dimension reduction analyses were performed on 6 years of morphometric data to assign breeding status to individuals. Three analytical approaches (GLMM, binomial logistic regression and multinomial logistic regression) were used to model the effects of breeding status on GRO in the current dataset and a historical dataset derived from previous studies of wild callitrichids. Though alloparents have long been considered critical to reproductive success in cooperative breeders, these results indicate that group size and the proportion of primary breeders are the most significant factors contributing to GRO. This indicates that reproductive suppression of subordinate females may even be detrimental to GRO and though additional primary breeding males increased GRO, the addition of secondary breeders, male or female, did not.