World Primates Research Articles

Compound grips in tufted capuchin monkeys (Sapajus spp and Sapajus libidinosus).

An experimental study with captive individuals and study of video recordings of wild monkeys explored whether and how tufted capuchin monkeys use onehand to hold one or more objects with multiple grips (compound grips). A task designed to elicit compound grip was presented to five captive tufted capuchin monkeys (Sapajus spp). The monkeys held one to four balls in onehand and dropped the balls individually into a vertical tube. Multiple simple grips and independent digit movements enabled separate control of multiple objects in one hand. Monkeys always supported the wrist on the horizontal edge of the tube before releasing the ball. Increasing the number of balls decreased the likelihood that the monkeys managed the task. Wild bearded capuchins (Sapajus libidinosus) used compound grips spontaneously to store multiple food items. Compound grips have been described in macaques, gorillas, chimpanzees, and humans, and now in a New World primate. We predict that any primate species that exhibits precision grips and independent digit movement can perform compound grips. Our findings suggest many aspects of compound grip that await investigation.

Looming and receding visual networks in awake marmosets investigated with fMRI

An object that is looming toward a subject or receding away contains important information for determining if this object is dangerous, beneficial or harmless. This information (motion, direction, identity, time-to-collision, size, velocity) is analyzed by the brain in order to execute the appropriate behavioral responses depending on the context: fleeing, freezing, grasping, eating, exploring. In the current study, we performed ultra-high-field functional MRI (fMRI) at 9.4T in awake marmosets to explore the patterns of brain activation elicited by visual stimuli looming toward or receding away from the monkey. We found that looming and receding visual stimuli activated a large cortical network in frontal, parietal, temporal and occipital cortex in areas involved in the analysis of motion, shape, identity and features of the objects. Looming stimuli strongly activated a network composed of portions of the pulvinar, superior colliculus, putamen, parietal, prefrontal and temporal cortical areas. These activations suggest the existence of a network that processes visual stimuli looming toward peripersonal space to predict the consequence of these stimuli. Together with previous studies in macaque monkeys, these findings indicate that this network is preserved across Old and New World primates.

A Muscle‐fiber Comparison in New World Monkeys Based on Brain Size, Body Mass and Locomotor Style

This study is part of a larger one (Muchlinski et al., 2018) focusing on the relationship between muscle mass and brain mass in primates with a specific focus on differential muscle fiber‐type distribution. Data from these studies can be used to address evolutionary questions in relation to the evolution of energetics and potential influences from body size and locomotory style. Primates have much larger brains than other non‐primate mammals, yet their overall metabolic requirements for body size are similar. When active, skeletal muscle is in direct competition with the brain for glucose and is an expensive tissue to maintain. Type I skeletal muscle fibers convert glucose to ATP using oxygen making them more energetically expensive. Previous studies demonstrated a negative correlation between brain size and type I fibers in lemuroidea (N=7) and hominoid primates (N=7), suggesting that as brain mass increases, type I fiber composition decreases. Based on these observations we hypothesized that platyrrhine primates would correspondingly have an increase in type II fibers in accordance to brain mass to account for more expensive tissue. Our goal was to measure type I and type II fiber distribution in New World primates using immunohistochemistry to develop a muscle fiber distribution profile. Two upper‐limb (deltoid and pectoralis major) and two hind‐limb muscles (gastrocnemius and soleus) were sampled from 5 New World primate taxa as well as the Philippine tarsier (N=7) that represented a range of body size and locomotory style. All samples were FFPE and sectioned (10um) for immunohistochemistry with a focus on type I and type II myosin heavy‐chain antibodies (abcam, 1:750). Stained sections were accessed for fiber‐type distribution using light microscopy and Image J, and multiple linear regression statistical analyses were performed. Overall larger‐brained primates displayed fewer type I fibers suggesting a negative correlation between brain mass and type I fibers. Deltoid fiber compositions quantified from T. syrichta (3.14cc), S. habiatus (cc), A. azazae (20.65cc) and S. apella (73.21cc), demonstrated a reduction in Type I fibers; 39.55%, 31.50%, 28.45% and 18.35% respectively, as endocranial volumes (ECV) increased. This observed trend was consistent across gastrocnemius and pectoralis major muscles. Conversely, the soleus of larger primates displayed a higher percentage of type I fibers (A. azazae; 71.61% and S. apella 81.76%) when compared with smaller primates (T. syrichta; 22.00%). Regression analysis of the platyrrhine primates produced a predictive model for ECV (R2 = 0.99 and RMSE = 2.3248) while the platyrrhine and hominoid data combined also demonstrated good prediction capabilities (R2 = 0.81 and RMSE = 83.074). The model found body mass (g), %fast‐twitch fibers and taxa to be the greatest explanatory variables in predicting brain size with body mass having the strongest effect. The present fiber distribution results are consistent with results from previous studies, and with the Expensive Tissue Hypothesis, however, the effects of body size and locomotory style cannot be discounted.Support or Funding InformationNational Science Foundation

Development of hepatic pathology in GBV-B-infected red-bellied tamarins (Saguinus labiatus).

GB virus B (GBV-B) is a new world monkey-associated flavivirus used to model acute hepatitis C virus (HCV) infection. Critical for evaluation of antiviral or vaccine approaches is an understanding of the effect of HCV on the liver at different stages of infection. In the absence of longitudinal human tissue samples at defined time points, we have characterized changes in tamarins. As early as 2 weeks post-infection histological changes were noticeable, and these were established in all animals by 6 weeks. Despite high levels of liver-associated viral RNA, there was reversal of hepatic damage on clearance of peripheral virus though fibrosis was demonstrated in four tamarins. Notably, viral RNA burden in the liver dropped to near undetectable or background levels in all animals which underwent a second viral challenge, highlighting the efficacy of the immune response in removing foci of replication in the liver. These data add to the knowledge of GBV-B infection in New World primates which can offer attractive systems for the testing of prophylactic and therapeutic treatments and the evaluation of their utility in preventing or reversing liver pathology.

Elaboration of the Corticosteroid Synthesis Pathway in Primates through a Multistep Enzyme.

Metabolic networks are complex cellular systems dependent on the interactions among, and regulation of, the enzymes in the network. Although there is great diversity of types of enzymes that make up metabolic networks, the models meant to understand the possible evolutionary outcomes following duplication neglect specifics about the enzyme, pathway context, and cellular constraints. To illuminate the mechanisms that shape the evolution of biochemical pathways, I functionally characterize the consequences of gene duplication of an enzyme family that performs multiple subsequent enzymatic reactions (a multistep enzyme) in the corticosteroid pathway in primates. The products of the corticosteroid pathway (aldosterone and cortisol) are steroid hormones that regulate metabolism and stress response in tetrapods. These steroid hormones are synthesized by a multistep enzyme Cytochrome P450 11B (CYP11B) that performs subsequent steps on different carbon atoms of the steroid derivatives. Through ancestral state reconstruction and in vitro characterization, I find that the primate ancestor of the CYP11B1 and CYP11B2 paralogs had moderate ability to synthesize both cortisol and aldosterone. Following duplication in Old World primates, the CYP11B1 homolog specialized on the production of cortisol, whereas its paralog, CYP11B2, maintained its ability to perform multiple subsequent steps as in the ancestral pathway. Unlike CYP11B1, CYP11B2 could not specialize on the production of aldosterone because it is constrained to perform earlier steps in the corticosteroid synthesis pathway to achieve the final product aldosterone. These results suggest that enzyme function, pathway context, along with tissue-specific regulation, both play a role in shaping potential outcomes of metabolic network elaboration.

Is the Loss of Trpc2 Gene Function a Real Working Hypothesis for the Emergence of Same-Sex Sexual Behavior in Old World Primates?

Is the Loss of Trpc2 Gene Function a Real Working Hypothesis for the Emergence of Same-Sex Sexual Behavior in Old World Primates?

Spontaneous color preferences in rhesus monkeys: What is the advantage of primate trichromacy?

Color perception and color signaling play an important role in various aspects of animal behavior. However, in mammals, trichromatic vision characterized by three retinal photopigments tuned to peak short, middle and long wavelengths is limited only to some primate species. In Old and New World primates a second photopigment has appeared repeatedly during phylogeny, allowing red colors to be distinguished from yellows and greens.Several hypotheses aspire to explain the adaptive benefits of trichromatic vision for primates. The predominant one is foraging adaptation for facilitation visual detection of fruits or young leaves. Alternative explanations are based on the function of red color in aposematic signaling or its role in socio-sexual communication.We tested spontaneous color preference in macaque monkeys (Macaca mulatta) for both food and non-food objects in a laboratory environment. We hypothesized that preference for or avoidance of red color together with the context of such behavior may help us to understand what the adaptive advantage leading to a rapid expansion of a gene for a second pigment in the long-wavelength region was.We found neither preference nor avoidance toward red color in non-food objects, but we found a significant preference for red color in food; therefore, we suggest that the results support the foraging hypothesis in macaque monkeys.

The characterization of two novel neotropical primate papillomaviruses supports the ancient within-species diversity model.

Papillomaviruses (PVs) are non-enveloped icosahedral viruses with a circular double-stranded DNA genome of ∼8,000 base pairs (bp). More than 200 different PV types have been identified to date in humans, which are distributed in five genera, with several strains associated with cancer development. Although widely distributed in vertebrates, Neotropical Primates (NP) PV infection was described for the first time only in 2016. Currently, four complete genomes of NP PVs have been characterized, three from Saimiri sciureus (SscPV1 to SscPV3) and one from Alouatta guariba (AgPV1). In this work, we describe two novel PV strains infecting Callithrix penicillata (provisionally named CpenPV1 and CpenPV2), using anal swab samples from animals residing at the Brasilia Primatology Center and next generation sequencing. The genomes of CpenPV1 (7,288 bp; 41.5% guanine-cytosine content - GC) and CpenPV2 (7,250 bp; 40.7% GC) contain the characteristic open reading frames (ORFs) for the early (E6, E7, E1, E2, and E4) and late (L2 and L1) PV genes. The L1 ORFs, commonly used for phylogenetic identification, share 76 per cent similarity with each other and differ 32 per cent from any other known PV, indicating that these new strains meet the criteria for defining novel species. PV genes phylogenetic variance was analyzed and different degrees of saturation revealed similar levels of topological heterogeneity, ruling out saturation as primary etiological factor for this phenomenon. Interestingly, the two CpenPV strains form a monophyletic clade within the Gammapapillomavirus genus (provisionally named gammapapillomavirus 32). Unlike for other NP PV strains, which grouped into a new sister genus of Alphapapillomavirus, this is the first report of NP PV strains grouping into a genus previously considered to exclusively comprise Old World Primates (OWP) PVs, including human PVs. These findings confirm the existence of a common ancestor for Gammapapillomavirus already infecting primates before the split of OWP and NP at ∼40 million years ago. Finally, our findings are consistent with an ancient within-species diversity model and emphasize the importance of increasing sampling to help understanding the PV-primate codivergence dynamics and pathogenic potential.

Geographical patterns and current and short‐term historical correlates of phylogenetic diversity and endemism for New World primates

AbstractAimAddressing the phylogenetic relationship among species has been insightful to understand evolutionary and biogeographical processes shaping the distribution of diversity across broad geographical gradients. Here we determine the geographical distribution and the variables correlated with the phylogenetic component of diversity and endemism for primates, as well as their relationships with the taxonomic component of diversity.LocationNew World.TaxonNew World monkeys, Platyrrhini.MethodsWe mapped primate occurrence in cells of 110 × 110 km. For each cell, we calculated phylogenetic diversity (PD) and endemism (PE), as well as how much these indices deviate from their expected values based on species richness (SR) and endemism (SE), respectively. Using simultaneous autoregressive models, we tested the effects of mean annual temperature, forest structure and climate history on the current patterns of primate phylogenetic diversity.ResultsWe found that most primate phylogenetic diversity is found in the tropical forests of South America. Tropical forests also present much higher PD and PE than predicted by SR and SE, respectively, demonstrating their importance in producing and maintaining primate phylogenetic diversity in the New World. Furthermore, regions presenting low SR and SE nevertheless show high PE, likely because these areas have witnessed the evolution of many clades occurring exclusively therein. Overall, mean annual temperature had the highest influence in explaining phylogenetic indices.Main conclusionsOur results suggest a strong influence of primate biogeography throughout the New World on the geographical distribution of the phylogenetic component of their diversity, with the Amazon, Atlantic Forest and Central America containing the greatest amount and endemism of phylogenetic diversity. Our study contributes to a better understanding of the dynamics underlying the geographical distribution of New World's primate diversity, especially in a phylogenetic context in which their biogeographical history has deeply affected current patterns of primate diversity in this region. Our results provide essential information for the conservation of primate evolutionary history, especially considering the forecast effects of habitat loss and climate change on the dynamics of tropical forests.

Motion Perception in the Common Marmoset.

Visual motion processing is a well-established model system for studying neural population codes in primates. The common marmoset, a small new world primate, offers unparalleled opportunities to probe these population codes in key motion processing areas, such as cortical areas MT and MST, because these areas are accessible for imaging and recording at the cortical surface. However, little is currently known about the perceptual abilities of the marmoset. Here, we introduce a paradigm for studying motion perception in the marmoset and compare their psychophysical performance with human observers. We trained two marmosets to perform a motion estimation task in which they provided an analog report of their perceived direction of motion with an eye movement to a ring that surrounded the motion stimulus. Marmosets and humans exhibited similar trade-offs in speed versus accuracy: errors were larger and reaction times were longer as the strength of the motion signal was reduced. Reverse correlation on the temporal fluctuations in motion direction revealed that both species exhibited short integration windows; however, marmosets had substantially less nondecision time than humans. Our results provide the first quantification of motion perception in the marmoset and demonstrate several advantages to using analog estimation tasks.

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins.

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, multiparasitic 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 3 years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explored variation in parasite prevalence across age and sex classes, test nonrandom 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), 10 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.

Sex differences in main olfactory system pathways involved in psychosexual function.

We summarize literature from animal and human studies assessing sex differences in the ability of the main olfactory system to detect and process sex-specific olfactory signals ("pheromones") that control the expression of psychosexual functions in males and females. A case is made in non primate mammals for an obligatory role of pheromonal signaling via the main olfactory system (in addition to the vomeronasal-accessory olfactory system) in mate recognition and sexual arousal, with male-specific as well as female-specific pheromones subserving these functions in the opposite sex. Although the case for an obligatory role of pheromones in mate recognition and mating among old world primates, including humans, is weaker, we review the current literature assessing the role of putative human pheromones (eg, AND, EST, "copulin"), detected by the main olfactory system, in promoting mate choice and mating in men and women. Based on animal studies, we hypothesize that sexually dimorphic effects of putative human pheromones are mediated via main olfactory inputs to the medial amygdala which, in turn, transmits olfactory information to sites in the hypothalamus that regulate reproduction.

Eco-Epidemiological Profile and Molecular Characterization of Simian Foamy Virus in a Recently-Captured Invasive Population of Leontopithecus chrysomelas (Golden-Headed Lion Tamarin) in Rio de Janeiro, Brazil.

Simian foamy viruses (SFV) infect a wide range of Old World and Neotropical primates (NP). Unlike Old World primates, little is known about the diversity and prevalence of SFV in NP, mainly from a free-living population. Phylogenetic analyses have shown that SFV coevolved with their hosts. However, viral strains infecting Leontopithecus chrysomelas did not behave as expected for this hypothesis. The purpose of this study was to determine the eco-epidemiological profile and molecular characterization of SFV in a recently captured invasive population of L. chrysomelas located in Niteroi/RJ using buccal swab as an alternative collection method. A prevalence of 34.8% (32/92) and a mean viral load of 4.7 log copies of SFV/106 cells were observed. With respect to time since capture, SFV prevalence was significantly higher in the group of animals sampled over 6 months after capture (55.2%) than in those more recently captured (25.4%) (p = 0.005). Infected solitary animals can contribute to SFV transmission between different groups in the population. SFV strains formed two distinct clades within the SFV infecting the Cebidae family. This is the first study to use buccal swabs as a tool to study SFV diversity and prevalence in a recently free-living NP population upon recent capture.

High susceptibility, viral dynamics and persistence of South American Zika virus in New World monkey species

South American Zika virus (ZIKV) recently emerged as a novel human pathogen, linked with neurological disorders. However, comparative ZIKV infectivity studies in New World primates are lacking. Two members of the Callitrichidae family, common marmosets (Callithrix jacchus) and red-bellied tamarins (Saguinus labiatus), were highly susceptible to sub-cutaneous challenge with the Puerto Rico-origin ZIKVPRVABC59 strain. Both exhibited rapid, high, acute viraemia with early neuroinvasion (3 days) in peripheral and central nervous tissue. ZIKV RNA levels in blood and tissues were significantly higher in New World hosts compared to Old World species (Macaca mulatta, Macaca fascicularis). Tamarins and rhesus macaques exhibited loss of zonal occludens-1 (ZO-1) staining, indicative of a compromised blood-brain barrier 3 days post-ZIKV exposure. Early, widespread dissemination across multiple anatomical sites distant to the inoculation site preceded extensive ZIKV persistence after 100 days in New and Old World lineages, especially lymphoid, neurological and reproductive sites. Prolonged persistence in brain tissue has implications for otherwise resolved human ZIKV infection. High susceptibility of distinct New World species underscores possible establishment of ZIKV sylvatic cycles in primates indigenous to ZIKV endemic regions. Tamarins and marmosets represent viable New World models for ZIKV pathogenesis and therapeutic intervention studies, including vaccines, with contemporary strains.

Bocaparvovirus,ErythroparvovirusandTetraparvovirusin New World Primates from Central America

Parvoviruses in the genera Bocaparvovirus (HBoV), Erythroparvovirus (B19) and Tetraparvovirus (PARV4) are the only autonomous parvoviruses known to be associated with human and non-human primates based on studies and clinical cases in humans worldwide and non-human primates in Asia and Africa. Here, the presence of these agents with pathogenic potential was assessed by PCR in blood and faeces from 55 howler monkeys, 112 white-face monkeys, 3 squirrel monkeys and 127 spider monkeys in Costa Rica and El Salvador. Overall, 3.7% (11/297) of the monkeys had HboV DNA, 0.67% (2/297) had B19 DNA, and 14.1% (42/297) had PARV4 DNA, representing the first detection of these viruses in New World Primates (NWP). Sex was significantly associated with the presence of HBoV, males having greater risk up to nine times compared with females. Captivity was associated with increased prevalence for PARV4 and when all viruses were analysed together. This study provides compelling molecular evidence of parvoviruses in NWPs and underscores the importance of future research aimed at understanding how these viruses behave in natural environments of the Neotropics and what variables may favour their presence and transmission.

Genetic differentiation and diversity of the Bolivian endemic titi monkeys, Plecturocebus modestus and Plecturocebus olallae.

The genetic variability of New World primates is still poorly documented. We present the first genetic study on two threatened endemic titi monkey species in northern Bolivia (Plecturocebus modestus and Plecturocebus olallae) using six microsatellite markers to investigate genetic structure and variability of 54 individuals from two wild populations. A low level of genetic diversity was found (34 alleles in the total sampled population). Locus 1118 presented the greatest number of alleles. The mean number of alleles per locus in the total population was 5.6 and the average heterozygosity was 0.38 (range 0.12-0.88). The FIS value for the total population using all microsatellite loci shows a statistically significant heterozygote deficit. The inbreeding coefficients (FIS) were positive and significantly different from zero (0.064 for P. olallae and 0.213 for P. modestus). The genetic differentiation between populations (FST) was moderate with a pair-wise FST estimate of 0.14. Population structure analyses assigned the two populations to two differentiated clusters (K = 2). These results suggest that these two species with very close distributional ranges arose from a single population, and that they remain in a process of genetic differentiation and speciation. This study further underlines the urgent need for conservation actions for both endemic primate species.

Distinguished primatologist address-moving from advocacy to activism: Changing views of primate field research and conservation over the past 40 years.

Field studies of wild nonhuman primates have grown exponentially over the past 40 years and our knowledge of primate behavior, ecology, and social, and mating systems has expanded greatly. However, we are facing a major extinction crisis with some 60% of all primate species listed as threatened and more than 75% of species with declining populations. The primary factor driving primate population decline is human population increase, which over the past 50 years has resulted in the unsustainable conversion and degradation of natural landscapes for industrial agriculture, the production of nonagricultural commodities for international trade, pastureland for cattle, dam construction, fossil fuel exploration, mining, and the construction of road networks and infrastructure to support large urban centers. Recent ecological modeling predicts that by the end of the century, the four primate-richest countries in the world will lose 32-78% of their existing primate habitat to agricultural expansion, and nine of the top 15 primate-richest countries are expected to have 80-100% of their primate species extinct or threatened with extinction. If we are going to save the world's primates, the time to act is now! Not only should all primate field research include a strong conservation component, but in addition we must actively join with our professional societies, zoos and research facilities, universities, conservation organizations, concerned business leaders, global citizens, like-minded political leaders, and grassroots organizations to inform, demand and direct governments, multinational corporations, and international organizations to engage in transformational change to protect biodiversity and seek environmental justice against those entities that actively destroy our planet. As the chief academic discipline dedicated to the study of primates, we must organize and collectively move from being advocates for primate conservation to becoming activists for primate conservation. This is a call to action.

Seroprevalence of Human Adenovirus Type 5 Neutralizing Antibody in Common Marmosets Determined by a New Set of Two Assays.

Preexisting neutralizing antibody (NAb) against human adenovirus serotype 5 (AdHu5) can reduce the immunogenicity of AdHu5 vector-based vaccine, thus inhibiting the host's immune response and utility of other homologous vectors. Common marmoset (Callithrix jacchus), a small new world primate, has attracted considerable attention for its potential as a preclinical research model of vaccine development. However, the prevalence of anti-AdHu5 NAb activity in common marmosets bred in China remains unknown. A recombinant adenovirus expressing luciferase and Zs Green reporter genes were constructed to detect NAb against rAdHu5 by flow cytometry (FCM) and chemiluminescence (CL) assay. Five of 25 marmosets (20%) presented AdHu5 NAb detectable by FCM. Four animals had low titer (1/16), while the fifth one reached 1/64. While by CL assay, 7 of 25 (28%) marmosets were anti-AdHu5 NAb positive. Four animals, two of whom were negative by FCM, also had low titer NAb (1/16), suggesting assay discrepancy at low levels. Two marmosets, 1/32 titer by CL, were at 1/16 by FCM. A single animal showed a high titer with both assays (1/128 and 1/64 by CL and FCM, respectively). The CL method was simpler, more sensitive, accurate, and stable. The low prevalence of preexisting anti-AdHu5 NAb in marmosets provides important background information on the feasibility and applicability of using marmosets as a preclinical research model for vaccine development.

Ecological indicators of mammal exposure to Ebolavirus.

Much of the basic ecology of Ebolavirus remains unresolved despite accumulating disease outbreaks, viral strains and evidence of animal hosts. Because human Ebolavirus epidemics have been linked to contact with wild mammals other than bats, traits shared by species that have been infected by Ebolavirus and their phylogenetic distribution could suggest ecological mechanisms contributing to human Ebolavirus spillovers. We compiled data on Ebolavirus exposure in mammals and corresponding data on life-history traits, movement, and diet, and used boosted regression trees (BRT) to identify predictors of exposure and infection for 119 species (hereafter hosts). Mapping the phylogenetic distribution of presumptive Ebolavirus hosts reveals that they are scattered across several distinct mammal clades, but concentrated among Old World fruit bats, primates and artiodactyls. While sampling effort was the most important predictor, explaining nearly as much of the variation among hosts as traits, BRT models distinguished hosts from all other species with greater than 97% accuracy, and revealed probable Ebolavirus hosts as large-bodied, frugivorous, and with slow life histories. Provisionally, results suggest that some insectivorous bat genera, Old World monkeys and forest antelopes should receive priority in Ebolavirus survey efforts.This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’.

Individual, social, and environmental factors affecting salivary and fecal cortisol levels in captive pied tamarins (Saguinus bicolor).

Pied tamarins (Saguinus bicolor) are endangered New World primates, and in captivity appear to be very susceptible to stress. We measured cortisol in 214 saliva samples from 36 tamarins and in 227 fecal samples from 27 tamarins, and investigated the effects of age, sex, pregnancy, rearing history, social status, weight, group composition, and enclosure type using generalized linear mixed models. There was no effect of age on either fecal or salivary cortisol levels. Female pied tamarins in late pregnancy had higher fecal cortisol levels than those in early pregnancy, or nonpregnant females, but there was no effect of pregnancy on salivary cortisol. Females had higher salivary cortisol levels than males, but there was no effect of rearing history. However, for fecal cortisol, there was an interaction between sex and rearing history. Hand-reared tamarins overall had higher fecal cortisol levels, but while male parent-reared tamarins had higher levels than females who were parent-reared, the reverse was true for hand-reared individuals. There was a trend towards lower fecal cortisol levels in subordinate individuals, but no effect of status on salivary cortisol. Fecal but not salivary cortisol levels declined with increasing weight. We found little effect of group composition on cortisol levels in either saliva or feces, suggesting that as long as tamarins are housed socially, the nature of the group is of less importance. However, animals in off-show enclosures had higher salivary and fecal cortisol levels than individuals housed on-show. We suggest that large on-show enclosures with permanent access to off-exhibit areas may compensate for the effects of visitor disturbance, and a larger number of tamarins of the same species housed close together may explain the higher cortisol levels found in tamarins living in off-show accommodation, but further research is needed.