Platyrrhine Species Research Articles

COVID-19 in a common woolly monkey (Lagothrix lagothricha): First evidence of fatal outcome in a nonhuman primate after natural SARS-CoV-2 infection.

Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was declared a pandemic by the World Health Organization in March 2020. Since then, viral spread from humans to animals has occurred worldwide. Nonhuman primates (NHPs) have been found to be susceptible to reverse-zoonosis transmission of SARS-CoV-2, but initial research suggested that platyrrhine primates are less susceptible than catarrhine primates. Here we report the natural SARS-CoV-2 infection of a common woolly monkey (Lagothrix lagothricha) from a wildlife rehabilitation center in Ecuador. The course of the disease, the eventual death of the specimen, and the pathological findings are described. Our results show the susceptibility of a new platyrrhine species to SARS-CoV-2 and provide evidence for the first time of a COVID-19-associated death in a naturally infected NHP. The putative route of transmission from humans, and implications for captive NHPs management, are also discussed. Given that common woolly monkeys are at risk of extinction in Ecuador, further understanding of the potential threat of SARS-CoV-2 to their health should be a conservation priority. A One Health approach is the best way to protect NHPs from a new virus in the same way that we would protect the human population.

From molecular variations to behavioral adaptations: Unveiling adaptive epistasis in primate oxytocin system.

Our primary objective was to investigate the variability of oxytocin (OT) and the GAMEN binding motif within the LNPEP oxytocinase in primates. We sequenced the LNPEP segment encompassing the GAMEN motif in 34 Platyrrhini species, with 21 of them also sequenced for the OT gene. Our dataset was supplemented with primate sequences of LNPEP, OT, and the oxytocin receptor (OTR) sourced from public databases. Evolutionary analysis and coevolution predictions were made followed by the macroevolution analysis of relevant amino acids associated with phenotypic traits, such as mating systems, parental care, and litter size. To account for phylogenetic structure, we utilized two distinct statistical tests. Additionally, we calculated binding energies focusing on the interaction between Callithtrix jacchus VAMEN and Pro8OT. We identified two novel motifs (AAMEN and VAMEN), challenging the current knowledge of motif conservation in placental mammals. Coevolution analysis demonstrated a correlation between GAMEN, AAMEN, and VAMEN and their corresponding OTs and OTRs. Callithrix jacchus exhibited a higher binding energy between VAMEN and Pro8OT than orthologous molecules found in humans (GAMEN and Leu8OT). The coevolution of AAMEN and VAMEN with their corresponding OTs and OTRs suggests a functional relationship that could have contributed to specific reproductive and adaptive behaviors, including paternal care, social monogamy, and twin births, prominent traits in Cebidae species, such as marmosets and tamarins. Our findings underscore the coevolution of taxon-specific amino acids among the three studied molecules, shedding light on the oxytocinergic system as an adaptive epistatic repertoire in primates.

Gestural communication in wild spider monkeys (Ateles geoffroyi)

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy’s spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals’ gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients’ attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

MAST: Phylogenetic Inference with Mixtures Across Sites and Trees.

Hundreds or thousands of loci are now routinely used in modern phylogenomic studies. Concatenation approaches to tree inference assume that there is a single topology for the entire dataset, but different loci may have different evolutionary histories due to incomplete lineage sorting (ILS), introgression, and/or horizontal gene transfer; even single loci may not be treelike due to recombination. To overcome this shortcoming, we introduce an implementation of a multi-tree mixture model that we call mixtures across sites and trees (MAST). This model extends a prior implementation by Boussau et al. (2009) by allowing users to estimate the weight of each of a set of pre-specified bifurcating trees in a single alignment. The MAST model allows each tree to have its own weight, topology, branch lengths, substitution model, nucleotide or amino acid frequencies, and model of rate heterogeneity across sites. We implemented the MAST model in a maximum-likelihood framework in the popular phylogenetic software, IQ-TREE. Simulations show that we can accurately recover the true model parameters, including branch lengths and tree weights for a given set of tree topologies, under a wide range of biologically realistic scenarios. We also show that we can use standard statistical inference approaches to reject a single-tree model when data are simulated under multiple trees (and vice versa). We applied the MAST model to multiple primate datasets and found that it can recover the signal of ILS in the Great Apes, as well as the asymmetry in minor trees caused by introgression among several macaque species. When applied to a dataset of 4 Platyrrhine species for which standard concatenated maximum likelihood (ML) and gene tree approaches disagree, we observe that MAST gives the highest weight (i.e., the largest proportion of sites) to the tree also supported by gene tree approaches. These results suggest that the MAST model is able to analyze a concatenated alignment using ML while avoiding some of the biases that come with assuming there is only a single tree. We discuss how the MAST model can be extended in the future.

Edge effects and social behavior in three platyrrhines.

Social behavior is a key adaptation for group-living primates. It is important to assess changes to social behavior in human-impacted landscape zones to better understand the impact of anthropogenic disturbance on primate species. We investigated social behavior rate and type in three species of platyrrhines across 100 m anthropogenic edge and interior zones of a fragmented forest in Costa Rica, La Suerte Biological Research Station (LSBRS). Following results from other sites, we predicted that spider monkeys (Ateles geoffroyi), capuchin monkeys (Cebus imitator) and howler monkeys (Alouatta palliata) would show lower rates and fewer types of social behavior in forest edge compared to interior. We collected 1341 h of instantaneous focal data from 2017 to 2023 across the three monkey species. We found mixed support for our predictions, with spider and capuchin monkeys modifying some but not all aspects of social behavior across forest zones at LSBRS. Spider monkeys had lower rates of social behavior and capuchin monkeys performed different types of social behaviors in forest edge compared to interior at LSBRS. In contrast, howler monkeys did not modify social behavior. Two out of three platyrrhine species altered their social behavior when in anthropogenic edges, indicating behavioral adjustment when in human-altered habitat areas at LSBRS.

Ecological and phylogenetic influences on limb joint kinematics in wild primates

Abstract Arboreal locomotion is precarious and places multiple challenges upon stability. Studies have shown that captive primates respond to narrower and steeper supports by flexing limb joints and adopting a compliant gait. We tested whether these same kinematic responses are adopted by wild primates freely ranging over a variety of supports in their natural habitats. We recorded five species of platyrrhines, five species of catarrhines, and four species of strepsirrhines with modified GoPro cameras and used remote measurement to quantify substrate characteristics. Video images were imported into ImageJ to measure the angular kinematics of limb joints during quadrupedal locomotion on a variety of arboreal supports. We statistically tested for associations between joint posture and substrate characteristics, and then disentangled the influence of phylogeny and substrate on limb joint kinematics using variation partitioning and redundancy analysis. Our results partially confirm previous kinematic studies and suggest variation in support orientation, more than diameter or compliance, influences quadrupedal gait kinematics. Phylogenetic relatedness explained more variation in the data than substrate properties. This suggests primates either prospectively choose relatively ‘safe’ substrates for locomotion, or that they possess locomotor adaptations independent of limb joint kinematics per se to overcome the challenges of the precarious arboreal environment.

Quantitative assessment of grasping strength in platyrrhine monkeys.

Despite the longstanding importance of grasping adaptations in theories of primate evolution, quantitative data on primate grasping strength remain rare. We present the results of two studies testing the prediction that callitrichines-given their comparative retreat from a small-branch environment and specialization for movement and foraging on tree trunks and large boughs-should be characterized by weaker grasping forces and underdeveloped digital flexor muscles relative to other platyrrhines. First, we directly measured manual grasping strength in marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri boliviensis), using a custom-constructed force transducer. Second, we reanalyzed existing datasets on the fiber architecture of forearm and leg muscles in 12 platyrrhine species, quantifying digital flexor muscle physiological cross-sectional area (i.e., PCSA, a morphometric proxy of muscle strength) relative to the summed PCSA across all forearm or leg muscles. Callithrix was characterized by lower mean and maximum grasping forces than Saimiri, and callitrichines as a clade were found to have relatively underdeveloped manual digital flexor muscle PCSA. However, relative pedal digital flexor PCSA did not significantly differ between callitrichines and other platyrrhines. We found partial support for the hypothesis that variation in predominant substrate usage explains variation in empirical measurements of and morphological correlates of grasping strength in platyrrhines. Future research should extend the work presented here by (1) collecting morphological and empirical metrics of grasping strength in additional primate taxa and (2) extending performance testing to include empirical measures of primate pedal grasping forces as well.

Assessing color cues of development, breeding status and reproductive condition in captive golden lion tamarins (Leontopithecus rosalia).

Color signals play an important role in intraspecific communication and are well studied in catarrhine primates, which exhibit uniform trichromatic vision that is well suited to detecting such signals. Platyrrhine primates exhibit polymorphic color vision with different individuals possessing different color vision types in most species. Intriguingly, some platyrrhine species exhibit bare faces, which are convergent with those of catarrhines. However, putative functions of bare-faced color signals in platyrrhines remain largely unexplored. We measured facial skin color of five captive golden lion tamarins (Leontopithecus rosalia) using color-calibrated digital photography and modeled these colors to the visual systems of the species. Our results show that facial coloration is different between infant and older adults and varies across reproductive condition, but not between breeding and nonbreeding adults. While preliminary, our study suggests that facial coloration may be involved in sociosexual signaling in golden lion tamarins, and provides intriguing evidence that we hope might stimulate more studies of bare-faced signaling in platyrrhines.

Mapping Retrotransposon LINE-1 Sequences into Two Cebidae Species and Homo sapiens Genomes and a Short Review on Primates.

This work focuses on the distribution of LINE-1 (a Long Interspersed Nuclear Element) in primates and its role during evolution and as a constituent of the architecture of primate genomes. To pinpoint the LINE-1 repeat distribution and its role among primates, LINE-1 probes were mapped onto chromosomes of Homo sapiens (Hominidae, Catarrhini), Sapajus apella, and Cebus capucinus (Cebidae, Platyrrhini) using fluorescence in situ hybridisation (FISH). The choice of platyrrhine species are due to the fact they are taxa characterised by a high level of rearrangements; for this reason, they could be a useful model for the study of LINE-1 and chromosome evolution. LINE-1 accumulation was found in the two Cebidae at the centromere of almost all acrocentric chromosomes 16–22 and on some bi-armed chromosomes. LINE-1 pattern was similar in the two species but only for chromosomes 6, 8, 10, and 18, due to intrachromosomal rearrangements in agreement with what was previously hypothesised as through g banding. LINE-1 interstitial accumulation was found in humans on the 1, 8, 9, 13–15, and X chromosomes; on chromosomes 8, 9, and 13–15, the signal was also at the centromeric position. This is in agreement with recent and complete molecular sequence analysis of human chromosomes 8 and some acrocentric ones. Thus, the hypothesis regarding a link between LINE-1 and centromeres as well as a link with rearrangements are discussed. Indeed, data analysis leads us to support a link between LINE-1 and inter- and intrachromosomal rearrangements, as well as a link between LINE-1 and structural functions at centromeres in primates.

Validating Urinary Neopterin as a Biomarker of Immune Response in Captive and Wild Capuchin Monkeys.

Non-invasive health monitoring is advantageous for wild and captive primate populations because it reduces the need for traditional invasive techniques (i.e., anesthetization) that can be stressful and potentially harmful for individuals. The biomarker neopterin is an emerging tool in primatology to measure immune activation and immunosenescence, however, most neopterin studies have focused on catarrhine species with little comparative work examining neopterin and health in platyrrhines. To address this gap, we validated a commercially available enzyme-linked immunosorbent assay (ELISA) to measure urinary neopterin in two types of capuchin monkeys, a wild population of white-faced capuchins (Cebus imitator) and a socially housed captive colony of tufted capuchins (Sapajus apella). We analytically validated methods for measuring urinary neopterin in two capuchin populations and demonstrated that two commonly-used methods to control for urine concentration—creatinine and specific gravity (SG)—produced highly concordant results. We also biologically validated these methods by examining variation in neopterin levels based on environment (captive and wild) and age, and changes in levels associated with immune-response. We found that neopterin increased after immune perturbation (rabies vaccine booster), varied by environmental condition, and mirrored expected trends in immune system ontogeny. Our results improve understanding of the innate immune system in platyrrhine species and suggest neopterin may be useful for non-invasive health monitoring in both captive and wild primates.

Follow Your Nose: Ontogeny of the Olfactory Duct in Primates

Most primates are characterized by orbital convergence, the displacement of the orbits toward the rostral midline. In platyrrhine primates and tarsiers, this convergence is so extreme that orbits meet in the midline at the apical interorbital septum. This produces a spatial separation of the anterior cranial fossa and the nasal cavity. The olfactory bulbs of the brain pass dorsal and then rostral to the orbits to reach the nasal cavity via a bony tube, the olfactory duct. Nerves are expected to constrain growth of musculoskeletal structures. We hypothesized that the network of olfactory nerves effectively tethers the olfactory bulbs to the mucosa of the nasal cavity, and the growth of facial structures in these primates results in rostral displacement of the olfactory bulbs through ontogeny. In addition, growth of the midface may be constrained by this functional relationship.This comparative analysis was based on 3D reconstructions of cranial structures in newborns and adults from representative platyrrhine species (e.g., Aotus nancymaae and Cebuella pygmaea) and tarsiers (Tarsius syrichta). Spatial relationships of the olfactory duct were estimated using endocasts based on conventional microCT scans. In addition, diffusion iodine contrast‐enhanced CT (diceCT) images were used to study Aotus nancymaae at multiple stages of ontogeny. DiceCT allowed us to reconstruct the actual position of olfactory bulbs relative to the olfactory duct and the distribution of olfactory nerves in the nasal cavity. 3DSlicer and Blender software were used to render 3D models. These data confirm our hypothesis that the rostral projection of the olfactory bulbs relative to the frontal lobes of the brain increases through ontogeny. In addition, the paths of olfactory nerves are diverted around the convergent eyes. The ontogenetic relationships occurring in platyrrhine and tarsier olfactory ducts have evolutionary implications for biological variation in the primate skull.

Natural SARS-CoV-2 Infection in a Free-Ranging Black-Tailed Marmoset (Mico melanurus) from an Urban Area in Mid-West Brazil

The emergence of spillover pathogens such as SARS-CoV-2 is a risk to vulnerable human populations. We report natural SARS-CoV-2 infection in a free-ranging adult female black-tailed marmoset (Mico melanurus) from an urban area of Cuiabá, Mato Grosso State, Brazil. The animal was found after a motor vehicle collision without previous clinical history. Necropsy confirmed polytrauma. Severe multifocal to coalescent haemorrhage and mild multifocal peribronchial lymphocytic hyperplasia were seen in lung sections. The alveolar septa were multifocally expanded by a few lymphocytes. Mild lymphocytic periportal hepatitis and interstitial nephritis were found. The lymphoid nodules of the large intestine showed marked lymphocytic hyperplasia. Infection by SARS-CoV-2 was established by viral RNA detection in a pool of nasopharyngeal and oropharyngeal swabs and liver samples. Immunohistochemistry detected the viral nucleocapsid protein in sections of lung, liver, spleen, lymph nodes and large intestine, and spike protein antigen in lung tissue. This is the first report of naturally occurring SARS-CoV-2 infection in a New World monkey. Platyrrhine species should be included as potential hosts of natural infection of SARS-CoV-2.

Identification and evolutionary analysis of papillomavirus sequences in New World monkeys (genera Sapajus and Alouatta) from Argentina.

In this study, we investigated the occurrence of papillomavirus (PV) infection in non-human primates (NHPs) in northeastern Argentina. We also explored their evolutionary history and evaluated the co-speciation hypothesis in the context of primate evolution. We obtained DNA samples from 57 individuals belonging to wild and captive populations of Alouatta caraya, Sapajus nigritus, and Sapajus cay. We assessed PV infection by PCR amplification with the CUT primer system and sequencing of 337 bp (112 amino acids) of the L1 gene. The viral sequences were analyzed by phylogenetic and Bayesian coalescence methods to estimate the time to the most common recent ancestor (tMRCA) using BEAST, v1.4.8 software. We evaluated viral/host tree congruence with TreeMap v3.0. We identified two novel putative PV sequences of the genus Gammapapillomavirus in Sapajus spp. and Alouatta caraya (SPV1 and AcPV1, respectively). The tMRCA of SPV1 was estimated to be 11,941,682 years before present (ybp), and that of AcPV1 was 46,638,071 ybp, both before the coalescence times of their hosts (6.4 million years ago [MYA] and 6.8 MYA, respectively). Based on the comparison of primate and viral phylogenies, we found that the PV tree was no more congruent with the host tree than a random tree would be (P > 0.05), thus allowing us to reject the model of virus-host coevolution. This study presents the first evidence of PV infection in platyrrhine species from Argentina, expands the range of described hosts for these viruses, and suggests new scenarios for their origin and dispersal.

Centromeric enrichment of LINE-1 retrotransposon in two species of South American monkeys Alouatta belzebul and Ateles nancymaae (Platyrrhini, Primates)

LINE-1 sequences have been linked to genome evolution, plasticity and speciation; however, despite their importance, their chromosomal distribution is poorly known in primates. In this perspective, we used fluorescence in situ hybridization (FISH) to map LINE-1 probes onto two representative platyrrhine species, Aotus nancymaae (Cebidae) and Alouatta belzebul (Atelidae), both characterized with highly rearranged karyotypes, in order to investigate their chromosomal distribution and role and to better characterize the two genomes. We found centromeric enrichment of LINE-1 sequences on all biarmed and acrocentric chromosomes co-localized with heterochromatin C-positive bands. This distribution led us to hypothesize that LINE 1 sequences may have a role in the centromere architecture and karyotype organization of platyrrhine genomes.

Parasites of Free-Ranging and Captive American Primates: A Systematic Review.

The diversity, spread, and evolution of parasites in non-human primates (NHPs) is a relevant issue for human public health as well as for NHPs conservation. Although previous reviews have recorded information on parasites in NHPs (Platyrrhines) in the Americas, the increasing number of recent studies has made these inventories far from complete. Here, we summarize information about parasites recently reported in Platyrrhines, attempting to build on earlier reviews and identify information gaps. A systematic literature search was conducted in PubMed, ISI Web of Science, and Latin American and Caribbean Health Sciences Literature (LILACS), and following the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines. Ninety-three studies were included after the screening process. Records for 20 genera of NHPs, including 90 species were found. Most of the studies were conducted on captive individuals (54.1%), and morphological approaches were the most used for parasite identification. The most commonly collected biological samples were blood and stool, and Protozoa was the most frequent parasite group found. There is still scarce (if any) information on the parasites associated to several Platyrrhine species, especially for free-ranging populations. The use of molecular identification methods can provide important contributions to the field of NHPs parasitology in the near future. Finally, the identification of parasites in NHPs populations will continue to provide relevant information in the context of pervasive habitat loss and fragmentation that should influence both human public health and wildlife conservation strategies.

Evolutionary analysis of the anti-viral STAT2 gene of primates and rodents: Signature of different stages of an arms race.

STAT2 plays a strategic role in defending viral infection through the signaling cascade involving the immune system initiated after type I interferon release. Many flaviviruses target the inactivation or degradation of STAT2 as a strategy to impair this host's line of defense. Primates are natural reservoirs for a range of disease-causing flaviviruses (e.g., Zika, Dengue, and Yellow Fever virus), while rodents appear less susceptible. We analyzed the STAT2 coding sequence of 28 Rodentia species and 49 Primates species. Original data from 19 Platyrrhini species were sequenced for the SH2 domain of STAT2 and included in the analysis. STAT2 has many sites whose variation can be explained by positive selection, measurement by two methods (PALM indicated 12, MEME 61). Both evolutionary tests significantly marked sites 127, 731, 739, 766, and 780. SH2 is under evolutionary constraint but presents episodic positive selection events within Rodentia: in one of them, a moderately radical change (serine > arginine) at position 638 is found in Peromyscus species, and can be implicated in the difference in susceptibility to flaviviruses within Rodentia. Some other positively selected sites are functional such as 5, 95, 203, 251, 782, and 829. Sites 251 and 287 regulate the signaling mediated by the JAK-STAT2 pathway, while 782 and 829 create a stable tertiary structure of STAT2, facilitating its connection with transcriptional co-activators. Only three positively selected sites, 5, 95, and 203, are recognized members who act on the interface between STAT2 and flaviviruses NS5 protein. We suggested that due to the higher evolutionary rate, rodents are, at this moment, taking some advantage in the battle against infections for some well-known Flaviviridae, in particular when compared to primates. Our results point to dynamics that fit with a molecular evolutionary scenario shaped by a thought-provoking virus-host arms race.

Dramatic decline in a titi monkey population after the 2016-2018 sylvatic yellow fever outbreak in Brazil.

Platyrrhini are highly vulnerable to the yellow fever (YF) virus. From 2016 to 2018, the Atlantic Forest of southeast Brazil faced its worst sylvatic YF outbreak in about a century, thought to have killed thousands of primates. It is essential to assess the impact of this epidemic on threatened primate assemblages to design effective conservation strategies. In this study, we assessed the impact of the 2016-2018 YF outbreak on a geographically isolated population of Near Threatened black-fronted titi monkeys (Callicebus nigrifrons) in two Atlantic Forest patches of the Santuário do Caraça, MG, Brazil. Extensive preoutbreak monitoring, conducted between 2008 and 2016, revealed that the home range and group sizes of the population remained stable. In 2016, the population size was estimated at 53-57 individuals in 11-12 groups. We conducted monitoring and playback surveys in 2019 and found that the population had decreased by 68% in one forest patch and completely vanished in the other, resulting in a combined decline of 80%. We discuss this severe loss of a previously stable population and conclude that it was highly likely caused by the YF outbreak. The remaining population is at risk of disappearing completely because of its small size and geographic isolation. A systematic population surveys of C. nigrifrons, along other sensible Platyrrhini species, is needed to re-evaluate their current conservation status.

Functional and ecological correlates of the primate jaw abductors.

While the adductor musculature of the primate jaw has been extensively analyzed within the context of dietary and social ecology, little is known about the corresponding muscles of jaw abduction. Nonetheless, these muscles significantly contribute to a species' maximum gape potential, and thus might constrain dietary niche diversity and impact social display behaviors. In this study, we quantify the architectural properties of the digastric (a jaw abductor) and lateral pterygoid (a jaw abductor and anterior translator) across a broad sample of male and female anthropoid primates. We test the hypothesis that the abductor musculature reflects specialization to dietary and behavioral ecology. Our sample comprises 14 catarrhine and 13 platyrrhine species spanning a wide range of dietary and social categories. All specimens were sharp dissected and muscles subsequently chemically digested using a standardized protocol. Our findings demonstrate that relative fascicle lengths within the lateral pterygoid (but not the digastric) are significantly greater within species that habitually consume larger food items. Meanwhile, canine length is more strongly associated with fascicle lengths in the digastric than in the lateral pterygoid, particularly within males. Neither dietary mechanical resistance nor the intensity of social competition relates to the size or architectural properties of the jaw abductors. These findings suggest that dietary-and to a lesser extent, socioecological-aspects of a primate's life history may be reflected in the architecture of these muscles, albeit to varying degrees. This underlines the importance of considering the complete masticatory apparatus when interpreting the evolution of the primate jaw.

Oropendola nest predation and rodent consumption by the black-capped capuchin (<i>Sapajus apella</i>) in the Manu Biosphere Reserve, Peru


 
 
 Capuchins (Cebus and Sapajus spp.) are generalist primates, occurring in most Neotropical forest types where they forage opportunistically (Sabbatini et al., 2008; Lynch Alfaro et al., 2012; Boubli et al., 2020). They exploit a diverse variety of food sources, such as fruit, seeds, arthropods and a wide array of vertebrate prey (Rose, 1997; Albuquerque et al., 2014; Watts, 2020). Their foraging strategy is highly resourceful and adaptive, and they are often considered important predators of nests (Canale and Bernardo, 2016; Watts, 2020), including those of caiman (Torralvo et al., 2017), coatis (Rose, 1997; Ferrari, 2009) and especially of birds (Watts, 2020). In this work, we report observations of a foraging event by the black-capped capuchin, Sapajus apella (Linnaeus, 1758), a widely distributed platyrrhine species, common across much of the Amazon basin (Boubli et al., 2020). This report involves the first record of nest predation of the russet-backed oropendola, Psarocolius angustifrons (von Spix, 1824), by a primate, as well as the predation of arboreal rice rats, Oecomys sp. (Thomas, 1906).
 
 

Validation of a method for quantifying urinary C-peptide in platyrrhine monkeys

Urinary C-peptide (UCP) is a biomarker for insulin that can be used as a non-invasive physiological measure of energy balance. Previous research has validated the use of UCP to quantify energy balance in catarrhines; however, there have been no such studies in platyrrhines. Validation is necessary in this lineage of primates as divergent evolution has resulted in varied organization of insulin genes. Here, we evaluate a method for quantifying UCP in platyrrhines to measure energetic expenditure, a key component of calculating energy balance. Urine samples were opportunistically collected from laboratory-housed tufted capuchins (Sapajus apella) during exercise activities. To examine the efficacy of using UCP as a means for assessing energetic condition, we analyzed urine samples collected before and after exercise. Urinary C-peptide concentrations were measured using a commercial C-peptide radioimmunoassay. We found that on average, UCP concentrations were 0.34 ng/mL lower after exercise than they were prior to exercise (range =0.04 to 0.71 ng/mL). The rateofenergy expenditureper unit time was greater when capuchins were exercising at faster speeds. Concordantly, UCP concentrations decreased more following exercise at those faster speeds. Parallelism of serial dilutions of samples was calculated to assess the precision of UCP concentrations produced using these methods. Measured UCP concentrations decreased at expected intervals in accordance with each dilution factor. Our results provide biological validation of the use of a commercial assay for quantifying UCP as a measure of energy expenditure in this platyrrhine species.