From pathology to pleasure: Reframing mechanistic studies on same-sex sexual behavior in primates.

Same-sex sexual behaviors (SSB) in primates have historically been studied as sexual perversions, evolutionary paradoxes, and hormone-driven pathologies. Researchers in recent decades have challenged these perspectives, yet some of the original biases still linger. In this paper, we examine how the study of endocrinological mechanisms in SSB has been influenced by the historical framework of pathology. Societal attitudes and cultural conceptions of human sexuality have led researchers to study SSB in primates as the outcome of "abnormal" processes of "feminization" or "masculinization" of sexual behavior. Here, we argue for a renewed attention to other areas of inquiry regarding the relationship between hormones and SSB, such as the role of pleasure. We briefly review how current knowledge on the neuroendocrinology of pleasure in nonhuman primates may relate to the expression of SSB and highlight oxytocin and dopamine as potentially fruitful areas for future research. We argue that future studies on SSB in primates would benefit from 1) acknowledging how the historical study of SSB as a pathology has shaped mechanistic studies and 2) studying SSB with the same holistic approach as is taken with different-sex sexual behavior (DSB).

Oxytocin increases during fur-rubbing regardless of level of social contact in tufted capuchin monkeys.

Social interactions induce oxytocin release in many social species, suggesting that oxytocin is a critical part of social bonding among individuals. However, oxytocin also increases as a result of physical contact and stimulation, making it unclear which features of affiliative behaviors (for instance, social interaction or physical contact with a conspecific) drive the oxytocin increase observed after engaging in these behaviors. We attempted to tease this apart by studying the differential effect of social interaction, visual coordination with a conspecific, and physical stimulation during the fur-rubbing behavior of tufted capuchin monkeys (Sapajus [Cebus] apella), which often involves social contact with groupmates but is in some cases performed alone. We induced fur-rubbing by providing onions under three conditions: when capuchins had physical access to their social group and fur-rubbed in contact with groupmates (social condition), when capuchins were separated from their social group but could still see them fur-rub (visual coordination), and when capuchins were physically and visually separated from their groupmates (physical stimulation only). We assessed urinary oxytocin in these three conditions and compared them to a control condition in which apples were provided and no fur-rubbing was observed. Capuchins fur-rubbed for less time when they could not see their groupmates, but fur-rubbing increased urinary oxytocin above the control condition in all three fur-rubbing conditions equally, suggesting that the physical stimulation derived from fur-rubbing was the most important driver of oxytocin increase. These results support a model in which physical stimulation is an important factor in the relationship between oxytocin and at least some behaviors, suggesting that oxytocin increase alone is not necessarily indicative of a social influence on behavior. Future work is needed to determine the contexts in which social factors do impact oxytocin, and whether the downstream behaviors are the same for socially and nonsocially induced oxytocin release.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

High density of white-faced capuchins (Cebus capucinus) and habitat quality in the Taboga Forest of Costa Rica.

Across the globe, primates are threatened by human activities. This is especially true for species found in tropical dry forests, which remain largely unprotected. Our ability to predict primate abundance in the face of human activity depends on different species' sensitivities as well as on the characteristics of the forest itself. We studied plant and primate distribution and abundance in the Taboga Forest, a 516-ha tropical dry forest surrounded by agricultural fields in northwestern Costa Rica. We found that the density of white-faced capuchins (Cebus capucinus) at Taboga is 2-6 times higher than reported for other long-term white-faced capuchin sites. Using plant transects, we also found relatively high species richness, diversity, and equitability compared with other tropical dry forests. Edge transects (i.e., within 100 m from the forest boundary) differed from interior transects in two ways: (a) tree species associated with dry forest succession were well-established in the edge and (b) canopy cover in the edge was maintained year-round, while the interior forest was deciduous. Sighting rates for capuchins were higher near water sources but did not vary between the edge and interior forest. For comparison, we also found the same to be true for the only other primate in the Taboga Forest, mantled howler monkeys (Alouatta palliata). Year-round access to water might explain why some primate species can flourish even alongside anthropogenic disturbance. Forest fragments like Taboga may support high densities of some species because they provide a mosaic of habitats and key resources that buffer adverse ecological conditions.

Urinary oxytocin in capuchin monkeys: Validation and the influence of social behavior.

In highly social species, like primates, oxytocin plays an important role in cooperation, and in the formation and maintenance of social relationships. Despite recent interest in the relationship between oxytocin and social behavior in nonhuman primates, relatively little is known about endogenous oxytocin in social New World Monkeys. In this paper, we investigate the relationship between oxytocin and affiliative behaviors in socially-housed captive capuchin monkeys (Sapajus [Cebus] apella) by first validating methods of analysis of urinary oxytocin in this species and, second, examining the effects of grooming and fur-rubbing behavior on oxytocin concentrations and further affiliative behavior. In the validation, we found that intranasal exogenous oxytocin significantly increased urinary oxytocin 15-60 min post-administration. Oxytocin was also implicated in both grooming and fur-rubbing behaviors. We found that oxytocin concentrations increased after subjects engaged in grooming or fur-rubbing. In addition, we found that fur-rubbing influenced affiliative behaviors, both during and after a social fur-rubbing bout. While individuals spent more time in contact and proximity while fur-rubbing, immediately following the fur-rubbing event (15-30 min afterwards) all affiliative behaviors decreased. This supports previous research that oxytocin may, in fact, initially be related to increased social distance in this species. Yet, an increase in all affiliative behaviors 30-45 min after the onset of fur-rubbing suggests that fur-rubbing, like grooming, may ultimately function to strengthen social relationships. Overall, these results support a critical role for oxytocin in affiliative behaviors that maintain and strengthen social relationships in capuchin monkeys, and highlight the complexity of the interactions among oxytocin, affiliative behaviors, and social bonding.

No evidence of attentional bias toward threatening conspecific and allospecific faces in capuchin monkeys (Sapajus [Cebus] apella) using a dot-probe task.

The ability to quickly perceive and interpret threatening facial expressions from others is critical for successfully maintaining group cohesion in social nonhuman primate species. Rapid detection of threatening or negative stimuli in the environment compared to neutral stimuli, referred to as an attentional bias toward threat, is adaptive in that faster threat detection can lead to greater survival outcomes. However, the evolutionary roots of attentional bias formation toward social threat are not well understood. The present study investigated attentional biases toward social threat and the factors associated with them, including underlying hormonal mechanisms, in socially housed capuchin monkeys. Attentional biases were assessed using a dot-probe task that measured capuchins' latency to respond to a target using a joystick after viewing threatening or neutral conspecific or allospecific faces or nonface stimuli. In our first study, we examined how age, dominance status, sex, and cortisol level related to attentional biases. In our second study, we examined how manipulated oxytocin (OT) influenced attentional biases. Capuchin monkeys did not show attentional biases toward threatening faces or objects, but they showed attentional avoidance of scrambled familiar conspecific face stimuli. Cortisol and social rank were associated with attentional bias toward threat in the capuchin monkeys that participated in this study, which suggests that stress and dominance relate to attentional bias toward social threat. Manipulated OT increased attentional avoidance of scrambled familiar and unfamiliar face images, but not unscrambled faces or objects. Overall, we did not find compelling evidence of attentional biases toward social threat in capuchin monkeys. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Animal Emotions and Consciousness: Researchers' Perceptions, Biases, and Prospects for Future Progress.

Do animals have emotions? Scientists and philosophers have long struggled with this question, with debates ranging from whether animals experience an "internal world" to whether we are capable of studying it. Recently, theoretical, and methodological advances have rekindled this debate, yet, it is unclear where the scientific consensus on these topics lies today. To address this gap, we administered a survey of professional animal behavior researchers to assess perceptions regarding (1) the taxonomic distribution of emotions and consciousness in non-human animals, (2) respondents' confidence in this assessment, and (3) attitudes towards potential for progress and possible pitfalls when addressing these questions. In general, animal behavior researchers (n=100) ascribed emotionality and consciousness to a broad swath of the animal taxa, including non-human primates, other mammals, birds, and cephalopods, with varying degrees of confidence. There was a strong positive relationship between how likely a respondent was to attribute emotions to a given taxa and their confidence in that assessment, with respondents assuming an absence of emotions and consciousness when they were unsure. In addition, respondents' assessments were shaped by several traits (e.g., advanced cognitive abilities, consciousness) that they also admitted were not necessary for an animal to experience emotions. Ultimately, a large majority of researchers were optimistic that tools either currently exist or will exist in the future to rigorously address these questions (>85%) and that animal behavior, as a field, should do more to encourage emotions research (71%). We discuss implications of our findings for publication bias, ethical considerations, and identify an emergent consensus for the need of a functional definition of emotions to facilitate future work.

Sex differences in white matter tracts of capuchin monkey brains.

Nonhuman primates exhibit sexual dimorphism in behavior, suggesting that there could be underlying differences in brain organization and function. Understanding this neuroanatomical variation is critical for enhancing our understanding of the evolution of sex differences in the human brain. Tufted capuchin monkeys (Sapajus [Cebus] apella) represent a phylogenetically diverse taxa of neotropical primates that converge on several behavioral characteristics with humans relevant to social organization, making them an important point of comparison for studying the evolution of sex differences in primates. While anatomical sex differences in gray matter have previously been found in capuchin monkeys, the current study investigates sex differences in white matter tracts. We carried out tract-based spatial statistical analysis on fractional anisotropy images of tufted capuchin monkeys (15 female, 5 male). We found that females showed significantly higher fractional anisotropy than males in regions of frontal-parietal white matter in the right cerebral hemisphere. Paralleling earlier findings in gray matter, male and female fractional anisotropy values in these regions were nonoverlapping. This complements prior work pointing toward capuchin sex differences in limbic circuitry and higher-order visual regions. We propose that these sex differences are related to the distinct socioecological niches occupied by male and female capuchins. Capuchin neuroanatomical sex differences appear to be more pronounced than in humans, which we suggest may relate to human adaptations for prolonged neurodevelopmental trajectories and increased plasticity.

Endogenous cortisol correlates with performance under pressure on a working memory task in capuchin monkeys.

Humans often experience striking performance deficits when their outcomes are determined by their own performance, colloquially referred to as "choking under pressure." Physiological stress responses that have been linked to both choking and thriving are well-conserved in primates, but it is unknown whether other primates experience similar effects of pressure. Understanding whether this occurs and, if so, its physiological correlates, will help clarify the evolution and proximate causes of choking in humans. To address this, we trained capuchin monkeys on a computer game that had clearly denoted high- and low-pressure trials, then tested them on trials with the same signals of high pressure, but no difference in task difficulty. Monkeys significantly varied in whether they performed worse or better on high-pressure testing trials and performance improved as monkeys gained experience with performing under pressure. Baseline levels of cortisol were significantly negatively related to performance on high-pressure trials as compared to low-pressure trials. Taken together, this indicates that less experience with pressure may interact with long-term stress to produce choking behavior in early sessions of a task. Our results suggest that performance deficits (or improvements) under pressure are not solely due to human specific factors but are rooted in evolutionarily conserved biological factors.

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.

Sex differences in the brains of capuchin monkeys (Sapajus [Cebus] apella).

This study reports an analysis of 20 T1-weighted magnetic resonance imaging scans from tufted capuchin monkeys (5 male, 15 female). We carried out a data-driven, whole-brain volumetric analysis on regional gray matter anatomy using voxel-based morphometry. This revealed that males showed statistically significant expansion of a region of the hypothalamus, while females showed significant expansion in a distributed set of regions, including the cerebellum, early visual cortex, and higher-order visual regions spanning occipital and temporal cortex. In order to elucidate the network connectivity of these regions, we employed probabilistic tractography on diffusion tensor imaging data. This showed that the female-enlarged regions connect with distributed association networks across the brain. Notably, this contrasts with rodent studies, where sex differences are focused in deep, ancestral limbic regions involved in the control of reproductive behavior. Additionally, in our data set, for several regions, male and female volumetric measures were completely nonoverlapping. This contrasts with human studies, where sex differences in cortical regions have been reported but are characterized by overlapping rather than divergent male and female values. We suggest that these results can be understood in the context of the different lifetime experiences of males and females, which may produce increased experience-dependent cortical plasticity in capuchins compared to rodents, and in humans compared to capuchins.

Evidence for mutual assessment in a wild primate.

In aggressive interactions, game theory predicts that animals should assess an opponent's condition relative to their own prior to escalation or retreat. Despite the benefits of such mutual assessment, few studies have been able to reject simpler assessment strategies. Here we report evidence for mutual assessment in a wild primate. Gelada (Theropithecus gelada) males have conspicuous loud calls that may function as a signal of male quality. "Leader" males with harems putatively use loud calls to deter challenges from non-reproductive "bachelor" males. By contrast, leader males pose no threat to each other and congregate in large groups for a dilution effect against bachelors. In playback experiments and natural observations, gelada males responded to loud calls according to both their own and their opponent's attributes. Although primates routinely classify others relative to themselves using individual attributes, this represents some of the first direct evidence for mutual assessment in primate signaling contests.