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Coevolution between signalers and receivers has played a significant role in the diversity of animal signals and sensory systems. Platyrrhines (monkeys in the Americas) exhibit a remarkable color vision polymorphism that may have been selected by both natural and sexual selection, but sociosexual color signaling among platyrrhines has received almost no attention. Here, we study the color of reproductive skin among different reproductive classes in free-ranging female saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins, modeling color spaces, and contrasts for the different visual systems. We find that the chromatic saturation and luminance of genital color vary between reproductive classes in saddleback tamarins. Chromatic contrast between the vulva and belly is lower in the parous females (PFs) relative to adult but not currently breeding females, while achromatic contrast is higher in PFs in saddleback tamarins relative to nonparous females. However, in emperor tamarins, genital color (saturation, hue, and luminance) does not vary between reproductive classes. Overall, genital skin color variation is present in tamarins and may play a role in sexual signaling. Nevertheless, the patterns are inconsistent between species, suggesting interspecific variation. Future studies should integrate the perceiver's behavioral responses and the physical and social signaling environments into comprehensive studies of communication as well as consider the role and interaction between multiple sensory modalities.

Leptospirosis is a bacterial zoonotic disease with multiple serogroups that infects wildlife and humans alike. Several studies have detected the presence of leptospiral antibodies in captive Neotropical primates, suggesting that they are asymptomatic carriers. However, the presence of antibodies in free-ranging primates and their potential role as reservoirs for this pathogen is not known. In this study, we used the Microscopic Agglutination Test (MAT) to screen two species of free-ranging tamarins for the presence of Leptospira antibodies using a panel of 21 serogroups. A total of 56 primates (26 Leontocebus weddelli and 30 Saguinus imperator) were screened at the Estacion Biologica Rio Los Amigos in Madre de Dios, Peru. MAT results with titres of ≥100 in single samples were considered seropositive. Prevalence ratios (PR) were estimated for age group, sex and host species identity. Overall, 51.8% (29/56) of animals were reactive for at least one Leptospira serogroup. Serogroups were distributed as follows: Iquitos (41.1%), Icterohaemorrhagiae (14.3%), Sejroe (3.6%), Autumnalis (1.8%) and Bataviae (1.8%). No significant differences (p > .05) were found for seropositivity frequencies among categories within assessed variables. These results suggest that free-ranging L. weddelli and S. imperator might serve as reservoirs for pathogenic Leptospira serogroups. Given increasing human-wildlife contact, future studies that test for active infection are required to determine potential transmission risks to humans.

Chemosignals are mediators of social interactions in mammals, providing con- and hetero-specifics with information on fixed (e.g. species, sex, group and individual identity) and variable (e.g. social, reproductive and health status) features of the signaler. Yet methodological difficulties of recording and quantifying odor signals, especially in field conditions, have hampered studies of natural systems. We present the first use of the Torion® portable gas chromatography-mass spectrometry (GC-MS) instrument for in situ chemical analysis of primate scents. We collected and analyzed swab samples from the scent-glands and skin from 13 groups (57 individuals) of two sympatric species of wild emperor tamarins, Saguinus imperator, and Weddell’s saddleback tamarins, Leontocebus weddelli (Callitrichidae). In total, 11 compounds of interest (i.e. probably derived from the animals) could be detected in the samples, with 31 of 215 samples containing at least one compound of interest. The composition of these 31 samples varied systematically with species, group, sex and breeding status. Moreover, we tentatively identified seven of the compounds of interest as methyl hexanoate, benzaldehyde, ethyl hexanoate, acetophenone, a branched C15 alkane, 4-methoxybenzaldehyde and hexadecan-1-ol. As the field of primate semiochemistry continues to grow, we believe that portable GC-MS instruments have the potential to help make progress in the study of primate chemosignaling in field conditions, despite limitations that we encountered. We further provide recommendations for future use of the Torion® portable GC-MS for in situ analyses.

Chemosignals are mediators of social interactions in mammals, providing con- and hetero-specifics with information on fixed (e.g., species, sex, group, and individual identity) and variable (e.g., social, reproductive, and health status) features of the signaler. Yet, methodological difficulties of recording and quantifying odor signals, especially in field conditions, have hampered studies of natural systems. We present the first use of the Torion® portable gas chromatography-mass spectrometry (GC-MS) instrument for in situ chemical analysis of primate scents. We collected and analyzed swab samples from the scent glands and skin from 13 groups (57 individuals) of two sympatric species of wild emperor tamarins, Saguinus imperator, and Weddell's saddleback tamarins, Leontocebus weddelli (Callitrichidae). In total, 11 compounds of interest (i.e., probably derived from the animals) could be detected in the samples, with 31 of 215 samples containing at least one compound of interest. The composition of these 31 samples varied systematically with species, group, sex, and breeding status. Moreover, we tentatively identified seven of the compounds of interest as methyl hexanoate, benzaldehyde, ethyl hexanoate, acetophenone, a branched C15 alkane, 4-methoxybenzaldehyde, and hexadecan-1-ol. As the field of primate semiochemistry continues to grow, we believe that portable GC-MS instruments have the potential to help make progress in the study of primate chemosignaling in field conditions, despite limitations that we encountered. We further provide recommendations for future use of the Torion® portable GC-MS for in situ analyses.

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.

This collection of protocols are examples of protocols used for education in high throughput sequencing with Oxford Nanopore Technology's MinION sequencer.

For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We examined whether the frequency of terrestrial activity correlated with study duration (a proxy for sampling effort), rainfall level (a proxy for food availability seasonality), and forest height (a proxy for vertical niche dimension). Terrestrial activity was recorded frequently for Callicebus and Plecturocebus spp., but rarely for Cheracebus spp. Terrestrial resting, anti-predator behavior, geophagy, and playing frequencies in Callicebus and Plecturocebus spp., but feeding and moving differed. Callicebus spp. often ate or searched for new leaves terrestrially. Plecturocebus spp. descended primarily to ingest terrestrial invertebrates and soil. Study duration correlated positively and rainfall level negatively with terrestrial activity. Though differences in sampling effort and methods limited comparisons and interpretation, overall, titi monkeys commonly engaged in a variety of terrestrial activities. Terrestrial behavior in Callicebus and Plecturocebus capacities may bolster resistance to habitat fragmentation. However, it is uncertain if the low frequency of terrestriality recorded for Cheracebus spp. is a genus-specific trait associated with a more basal phylogenetic position, or because studies of this genus occurred in pristine habitats. Observations of terrestrial behavior increased with increasing sampling effort and decreasing food availability. Overall, we found a high frequency of terrestrial behavior in titi monkeys, unlike that observed in other pitheciids.

The establishment of baseline data on parasites from wild primates is essential to understand how changes in habitat or climatic disturbances will impact parasite-host relationships. In nature, multi-parasitic infections of primates usually fluctuate temporally and seasonally, implying that the acquisition of reliable data must occur over time. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over three years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explore variation in parasite prevalence across age and sex classes, test non-random associations of parasite co-occurrence, and assess the relationship between group size and PSR. From 288 fecal samples across 105 individuals (71 saddleback and 34 emperor tamarins), ten parasite taxa were identified by light microscopy following centrifugation and ethyl-acetate sedimentation. Of these taxa, none were host-specific, Dicrocoeliidae and Cestoda prevalences differed between host species, Prosthenorchis and Strongylida were the most prevalent. Host age was positively associated with Prosthenorchis ova and filariform larva, but negatively with cestode and the Rhabditoidea ova. We detected no differences between expected and observed levels of co-infection, nor between group size and parasite species richness over 30 group-years. Logistic models of individual infection status did not identify a sex bias; however, age and species predicted the presence of four and three parasite taxa, respectively, with saddleback tamarins exhibiting higher PSR. Now that we have reliable baseline data for future monitoring of these populations, next steps involve the molecular characterization of these parasites, and exploration of linkages with health parameters.

Genetic research is a rapidly evolving field of study that is increasingly being utilized as a tool for wildlife conservation. However, researchers and science educators in remote areas can often find it difficult to access the latest genetic technologies, often due to a combination of high costs, bulky equipment, and lack of infrastructure. Recent technological innovations are resulting in portable, low-cost instruments that enable next-generation sequencing in remote environments, offering new opportunities to generate a more widespread network of trained conservation scientists, particularly within regions of high biodiversity. What is currently lacking are formalized educational efforts to teach participants in biodiverse areas with hands-on training in molecular biology and real-time DNA sequencing techniques. To address this challenge, we report the design and summarized feedback/outcomes of a conservation genetics field course, called ‘Genomics in the Jungle’, that took place at a field research station in the Amazon rainforest of southeastern Peru. The program was established by a small US-based NGO, Field Projects International, and facilitated by a local eco-tourism company in Peru, Inkaterra. We utilized portable sequencing technologies from Oxford Nanopore Technologies, and in-kind support from the manufacturers MiniPCR, MiniOne Systems, Promega, and New England Biolabs. Participants included a mix of non-Peruvian students and local/regional students, some of which had no prior exposure to a genetics laboratory. Overall, we maintain that portable sequencing technology is democratizing scientific research and conservation efforts, and is a major step forward for science educators and conservationists.

This protocol is was used to conduct DNA 16S metagenomics on FPI's Genomics in the Jungle - 2018 field course at the Green Lab, located and Inkaterra Guides Field Station, Madre de Dios, Peru.

This protocol is was used to conduct DNA 18S metagenomics on FPI's Genomics in the Jungle - 2018 field course at the Green Lab, located and Inkaterra Guides Field Station, Madre de Dios, Peru.

This protocol is was used to conduct DNA 16S metagenomics on FPI's Genomics in the Jungle - 2018 field course at the Green Lab, located and Inkaterra Guides Field Station, Madre de Dios, Peru.

This protocol begins with blood stored in Longmire's solution and has as its goal, the sequencing of genomic DNA from several individuals onto a single MinION sequencing run. It is based on a protocol outlined by Thrasher et al. (2018) for the same process on a large number of warbler samples, but it differs from this original protocol in a few key ways: Since we ultimately were targeting sequencing by a MinION sequencer, the ultimate processing steps reflect library preparation for runs on this device, instead of Illumina sequencers. For the same reason, we also size selected larger fragments than can be sequenced on a MiSeq platform. This protocol is also meant to only analysed a few individuals (20 or less) since the MinION read coverage is lower than that of a MiSeq. The entire protocol was carried out in a field laboratory in the southeastern Peruvian Amazon, and therefore many of the luxuries a institutional laboratory can afford were not present to us We used gel-based size selection in the absence of methods such as Blue Pippin. We stored blood on FTA cards and in Longmire's solution in our sampling program. We discovered that yields from FTA cards, regardless of including large numbers of hole punches per extraction, simply were too low for the sequencing goals of this project. Therefore, we include the protocol of a WGA amplification step for these low samples. Longmire's solution produced higher yields, but some times, multiple extractions might need to be pooled together with an SPRI bead cleanup to be fully effective.

Social complexity may drive complexity in communicative systems due to an individual's need to navigate unpredictable interactions with multiple conspecifics. Cooperative breeding primates (marmosets and tamarins; family: Callitrichidae) live in groups with moderate to high reproductive skew, particularly in females, whereby sexually mature individuals are frequently prevented from breeding. Remarkably, dispersal from natal groups is not stereotyped upon reaching reproductive maturity. Individuals are often observed remaining in their natal groups until the same-sex breeder in their group or a neighboring group dies, experiencing hormonal reproductive suppression, aggression, and limited access to potential mates. Here we examined whether emperor tamarins (Saguinus imperator) might use vocal signals to reduce dispersal risks and maximize the likelihood of attaining a breeding position. Using six consecutive years of mark-recapture data, we showed that sexually mature non-breeders (herein "secondary breeders") are more likely to leave their groups from one year to the next than sexually mature breeders ("primary breeders"). This confirmed that, unlike primary breeders who do not need to disperse in order to reproduce, secondary breeders are choosing to accept the risks associated with dispersal and emigrating from their natal groups. We used neural networks to classify vocalizations according to individual breeding status, and conducted a series of playback experiments which demonstrated that tamarins discriminated between the calls of primary and secondary breeders. Our data support the hypotheses that secondary breeders disperse to increase mating opportunities and use vocalizations to signal their availability to potential mates. This species of cooperative breeder appears to use vocalization to navigate its social and reproductive systems, minimizing risks of dispersal and in turn increasing the likelihood of reproductive success. This research has important implications for our understanding of sexual signaling, partner choice, and reproductive success in cooperative breeders.

Noninvasive monitoring of gastrointestinal parasites from wild primates demonstrates that parasite-host relationships are altered during habitat or climatic disturbances. Interpreting changes in parasite measures for population health monitoring is problematic, since wild primates are infected with multiple parasites that fluctuate temporally and seasonally. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over three years to: 1) establish baseline levels of parasite species richness (PSR) and variation across demography; 2) test for non-random associations of parasite co-occurrence; and 3) test hypothesized relationships between group size and PSR. Ten distinguishable parasite taxa were identified from 288 fecal samples by light microscopy following centrifugation and ethyl-acetate sedimentation. These samples represented 105 unique individuals (71 saddleback and 34 emperor tamarins), across 13 saddleback and seven emperor groups. Of the parasites identified in this study, none were confirmed as host specific, and only two parasites had statistically different prevalence between the host species. With few exceptions, individual infection status remained relatively unchanged over the study period. Considering yearly pair-wise parasite associations, we detected no marked differences between expected and observed levels of co-infection, nor did we detect statistically significant associations between group size and parasite species richness over 30 group-years. Logistic models of individual infection status did not identify a sex bias; however, age or species predicted the presence of four and three parasite taxa, respectively. Our model found higher PSR for saddleback tamarins. Considering the two most common parasites, one is typically pathogenic and the other is not, reinforcing caution when translating clinical findings of pathology to real-world systems. We now have reliable baseline data for future monitoring of these populations. Next steps should involve the molecular characterization of these parasites, and the exploration of linkages with health parameters.

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 call's 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 network's 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.

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., Graphical abstract Image 1, Highlights • Co-infection data improves statistical models of parasite prevalence. • Longitudinal sampling is key to unraveling parasite-host relationships in nature. • Host specificity of blood parasites among sympatric Callitrichine primates. • Sex roles in cooperatively breeding primates may not impact parasitism.

Geophagy, or soil consumption, has been documented in diverse animal taxa, including many primates. Physiological functions such as mineral supplementation, detoxification of secondary compounds, and antacid properties are possible causes for this behavior. We report on observations of geophagy at arboreal termitaria by free-ranging Pithecia rylandsi at La Estacion Biologica Los Amigos (EBLA) in Peru between 2008 and 2015. Characteristics of geophagy events, including saki monkey behavior at the termitaria, were recorded and geochemical analyses were conducted on consumed termitaria, nearby topsoils, and unvisited termitaria. We observed 76 feeding bouts at 26 different termitaria by two groups of P. rylandsi during 1125 observational hours (0.07 bouts/obs. h). Geophagy occurred throughout the year, but rates peaked in January during the rainy season. All age and sex classes visited both active and inactive mounds. Feeding bouts were brief (171 ± SD 154 s), and no differences were observed in time spent feeding at active or inactive termitaria. Analyses showed that consumed soils contained higher concentrations of phosphorous, potassium, calcium, and magnesium than did topsoil. Consumed soils also contained a higher total cation exchange capacity than topsoil. Our analysis of consumed versus control termitaria revealed no differences in their chemical composition. We discuss these results in the context of the two primary hypotheses proposed for geophagy in pitheciins: mineral supplementation and toxin adsorption. Our data are consistent with the interpretation that P. rylandsi consume soils from arboreal termitaria to aid in adsorption of toxins found in immature seeds, which are a year-round component of their diet.

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.

There is a general consensus on the geographic distributions of many primate species; however, the continuity and validity of species range maps are often inaccurate on a local scale. In the case of rare and cryptic species, census methodology is often insufficiently rigorous or specialized, resulting in probable false negatives. Callimico goeldii is a rare primate, with most of its geographical range purported to lie in Peru. We evaluate the accuracy of its predicted geographic range within Peru with an assessment of mammal surveys over the last 40 yr and the inclusion of new sightings from three sites. We found that of all 340 study sites, only 10.9 % indicate that this species is present, and only 51 % of these sites receive any government protection. The Sierra del Divisor Reserve Zone and the Rodal Tahuamanu Conservation Concession have the highest estimated densities of Callimico goeldii. We suggest using focal follows of sympatric tamarins and vocalization playbacks rather than traditional line transects to improve the likelihood of locating this species. Although the current range maps based on the available data are likely an exaggeration of the species’ true range, the inherent imperfections of standard census methodology when applied to rare and cryptic species can lead to underrepresentative range maps as well. For these reasons, it is clear that the current distribution map for Callimico goeldii is imprecise, and until its distribution is reassessed, its conservation status cannot be confirmed.