Testing the effect of oxytocin on social grooming in bonobos.

Oxytocin has attracted research attention due to its role in promoting social bonding. In bonobos and chimpanzees, the two species most closely related to humans, urinary oxytocin is known to correlate with key behaviours related to social bonding such as social grooming in chimpanzees and female-female sexual behaviour in bonobos. However, no study has demonstrated that the administration of oxytocin promotes real-life social interactions in Pan, leaving it unclear whether oxytocin is merely correlated with social behaviors or does affect them in these species. To test this, we administered nebulized oxytocin or saline placebo to a group of female bonobos and subsequently observed changes in their gross behavior during free interaction. We found an overall effect of more frequent grooming in the oxytocin condition. However, on the individual level this effect remained significant for only one participant in our follow-up models, suggesting future work should explore interindividual variation. Our results provide some experimental support for the biobehavioural feedback loop hypothesis, which posits that some functions of the oxytocin system support the formation and maintenance of social bonds through a positive feedback loop; however, further tests with a larger number of individuals are required. Our results, at a minimum, demonstrated that oxytocin affects spontaneous, naturalistic social interactions of at least some female bonobos, adding to accumulating evidence that oxytocin modulates complex social behaviors of Pan.

Chimpanzees (Pan troglodytes) exhibit gaze bias for snakes upon hearing alarm calls.

Calls of several species of nonhuman animals are considered to be functionally referential. However, the cognitive mechanisms underlying audience behaviors remain unclear. This study used an audiovisual cross-modal preferential-looking paradigm to examine whether captive chimpanzees spontaneously associated a conspecific call with images of a corresponding item. Chimpanzees were presented with videos of snakes and fruit side-by-side while hearing playbacks of alarm calls, food-associated calls, or no sound (as a baseline condition). Chimpanzees looked at videos of snakes for longer when hearing alarm calls compared with food calls or baseline. However, chimpanzees did not look at videos of fruit for longer when hearing food calls compared with baseline. An additional experiment tested whether chimpanzees' gaze bias to the snake videos was driven by negative affective states in general via affect-driven attention biases. When chimpanzees were presented with the same snake and fruit videos while hearing playbacks of conspecific screams or no sound, they exhibited no gaze bias for snake videos. These results suggest that chimpanzees spontaneously associated alarm calls with images of a potential threat in a preferential-looking experiment and that this response was not simply driven by an affective state matching process. These findings should be interpreted in consideration of a procedural limitation related to pseudoreplication in the experimental stimuli. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Divergent effects of oxytocin on eye contact in bonobos and chimpanzees.

Oxytocin has drawn significant research attention for its role in modulating mammalian social behavior. Despite generally conserved roles, oxytocin can function differently even in closely related species. Previous studies have shown that bonobos and chimpanzees, humans' two closest relatives, demonstrate considerable behavioral differences, including that bonobos look more at others' eyes than chimpanzees. Oxytocin is known to increase attention to another's eyes in many mammalian species (e.g. dogs, monkeys, and humans), yet this effect has not been tested in any nonhuman great ape species. This study examined how intranasally-administered oxytocin affects eye contact in bonobos and chimpanzees using eye tracking. Following administration of either oxytocin or saline control with a nebulizer, chimpanzees (n = 6) and bonobos (n = 5) were shown images of conspecific faces while their eye movement was recorded. Oxytocin changed the eye-looking behavior of bonobos and chimpanzees differently. We found that oxytocin increased eye contact in bonobos but not chimpanzees; while one chimpanzee showed an increase, interestingly, 5 out of 6 chimpanzees showed decreased looking to the eyes compared to the mouth, suggesting moderate eye avoidance. Given the importance of eye contact in their social interactions, our results suggest that oxytocin may play modulatory roles in bonobos' and chimpanzees' species-specific social behavior and underscore the importance of oxytocin in hominid social evolution.

Comparative analysis of sperm motility in liquid and seminal coagulum portions between Bornean orangutan (Pongo pygmaeus) and chimpanzee (Pan troglodytes).

Coagulum in the semen of some primates plays different roles, depending on the species. In the present study, we examined sperm motility in the coagulum and liquid portions of semen collected from captive individuals from two great ape species: two adult Bornean orangutans (Pongo pygmaeus) (n = 27) and three adult chimpanzees (Pan troglodytes) (n = 14). The results revealed that orangutan sperm remained motile for significantly longer in the coagulum than in the liquid portion (> 18 h). By contrast, chimpanzee sperm motility did not differ significantly over time between the two portions of the semen, although motility was slightly higher in the liquid portion than in the coagulum. The evolution of the seminal coagulum is thought to be related to postcopulatory sperm competition; however, functions of seminal coagulum have not been completely elucidated. Our data from the orangutan semen suggest that in this species, seminal coagulum may strengthen own-sperm survival. This report is the first to provide evidence for this distinctive function of the seminal coagulum. This unique property of orangutan seminal coagulum might be attributable to their reproductive traits, e.g., difficulty in predicting ovulation due to a lack of genital swelling during estrus. The orangutan is a Critically Endangered species, and captive breeding, including artificial insemination (AI), is expected. However, worldwide, only one case of orangutan AI has been successful. Our findings may contribute to an understanding of their basic semen characteristics and help improve the AI method.

Social responses of travelling finless porpoises to boat traffic risk in Misumi West Port, Ariake Sound, Japan.

Anthropogenic effects have created various risks for wild animals. Boat traffic is one of the most fatal risks for marine mammals. Individual behavioral responses of cetaceans, including diving behavior such as changing swimming direction and lengthing inter-breath interval, to passing boats is relatively well known; however, the social function of cetacean responses to boat traffic in a natural setting remains poorly understood. We focused on describing the behavioral responses of single and aggregated finless porpoises to boats passing at Misumi West Port, Ariake Sound, Japan, by using a drone characterized with a high-precision bird's-eye angle. During the study period, we collected 25 episodes of finless porpoise responses to boats passing by. A mean (± SEM) of 5.1 ± 1.0 individuals were observed for each episode. The primary response to passing boats was avoidance by dive, which implies boat traffic is a substantial disturbance to finless porpoises that travel along the seawater surface daily. The diving duration decreased significantly with an increase in the number of aggregated individuals. The diving and floating reaction times were 10.9 ± 2.3 s and 18.7 ± 5.0 s, respectively. There was no significant difference between the reaction times indicating that each individual was motivated to keep the group cohesion consistent when floating even after the risk had dissolved, which is comparable to the behavior of porpoises that dive when riskier conditions are present, such as when a boat approaches an aggregation. Our findings provide new insights on the sociality of finless porpoises even though there were limitations, like an inability to identify a specific individual. The drone enabled us to observe the social behavior of finless porpoises and other cetaceans at an unprecedented resolution, which may lead to a better understanding of the evolutionary diversity of intelligence and sociality and the bridge to human evolution.

Social relationship and hair cortisol level in captive male chimpanzees (Pan troglodytes).

Understanding how social relationships affect long-term stress is important because stress has a profound impact on the welfare of animals and social relationships often exert a strong influence on their stress responses. The purpose of this study was to investigate the relationship between social behaviors and long-term stress levels as assessed by hair cortisol (HC) concentration. The subjects were 11 chimpanzees living in an all-male group (divided into two sub-groups) in Kumamoto Sanctuary, Kyoto University, Japan. Behavioral data were collected between December 2014 and March 2015. The total observation time was 129 h. Hair samples were collected in late March and early April 2015, and cortisol was extracted from the hair and measured with enzyme immunoassay. The hair growth rate was estimated to be 1.33 ± 0.06 cm/month. The results revealed that there was a positive correlation between the rate of receiving aggression and HC levels. We also found a significant negative correlation between the balance between giving and receiving grooming (grooming balance index: GBI), which was calculated by subtracting the rate with which grooming is given from that with which it is received, and the rate of receiving aggression and between the GBI and HC levels. Thus, individuals receiving higher levels of aggression also tended to give grooming for relatively long periods compared to the time they were being groomed. In contrast, the rate of initiating aggression did not have a relationship with either HC levels or any measure of social grooming. We did not find social buffering effects, as there was no correlation between mutual social grooming and HC levels. These results show that not only aggressive interactions but also overall social situations in which animals do not have balanced relationships with others might result in the long-term elevation of cortisol levels in captive male chimpanzees.

Chimpanzee Down syndrome: a case study of trisomy 22 in a captive chimpanzee.

We report a case of chimpanzee trisomy 22 in a captive-born female. Because chromosome 22 in great apes is homologous to human chromosome 21, the present case is analogous to human trisomy 21, also called Down syndrome. The chimpanzee in the present case experienced retarded growth; infantile cataract and vision problems, including nystagmus, strabismus, and keratoconus; congenital atrial septal defect; and hypodontia. All of these symptoms are common in human Down syndrome. This case was the second reported case of trisomy 22 in the chimpanzee. The chimpanzee in our case became blind by 7 years old, making social life with other chimpanzees difficult, but opportunities to interact with other conspecific individuals have been offered routinely. We believe that providing her with the best care over the course of her life will be essential.

Effects of Relocation and Individual and Environmental Factors on the Long-Term Stress Levels in Captive Chimpanzees (Pan troglodytes): Monitoring Hair Cortisol and Behaviors.

Understanding the factors associated with the long-term stress levels of captive animals is important from the view of animal welfare. In this study, we investigated the effects of relocation in addition to individual and environmental factors related to social management on long-term stress level in group-living captive chimpanzees by examining behaviors and hair cortisol (HC). Specifically, we conducted two studies. The first compared changes in HC levels before and after the relocation of 8 chimpanzees (Study 1) and the second examined the relationship between individual and environmental factors and individual HC levels in 58 chimpanzees living in Kumamoto Sanctuary (KS), Kyoto University (Study 2). We hypothesized that relocation, social situation, sex, and early rearing conditions, would affect the HC levels of captive chimpanzees. We cut arm hair from chimpanzees and extracted and assayed cortisol with an enzyme immunoassay. Aggressive behaviors were recorded ad libitum by keepers using a daily behavior monitoring sheet developed for this study. The results of Study 1 indicate that HC levels increased during the first year after relocation to the new environment and then decreased during the second year. We observed individual differences in reactions to relocation and hypothesized that social factors may mediate these changes. In Study 2, we found that the standardized rate of receiving aggression, rearing history, sex, and group formation had a significant influence on mean HC levels. Relocation status was not a significant factor, but mean HC level was positively correlated with the rate of receiving aggression. Mean HC levels were higher in males than in females, and the association between aggressive interactions and HC levels differed by sex. These results suggest that, although relocation can affect long-term stress level, individuals' experiences of aggression and sex may be more important contributors to long-term stress than relocation alone.

Analysis of hair cortisol levels in captive chimpanzees: Effect of various methods on cortisol stability and variability.

Hair cortisol has been reported to be a useful measure of long-term hypothalamic-pituitary-adrenal (HPA) axis activation in several species. It serves as a practical tool for long-term stress assessment, but it is important to understand the methodological factors that can affects hair cortisol assays to avoid methodological artifacts. To that end, we tested several procedures for measuring cortisol levels in hair collected from captive chimpanzees. The results showed that reproducibility was high, and we found no differences in cortisol levels among the various storage, drying, and sampling methods. However, the fineness of homogenized hair, sample weight, and extraction time affected absolute hair cortisol concentration. Although hair cortisol levels were stable over time, factors that may influence measurement results should be kept constant throughout a study.•We modified and validated a methodology involving enzyme immunoassays to reliably measure the hair cortisol levels of captive chimpanzees.•The results revealed that the fineness of homogenized hair, sample weight, and extraction time caused variations in absolute hair cortisol concentrations in chimpanzees. In contrast, storage, drying, and sampling from similar body parts did not affect the results.

Cortisol analysis of hair of captive chimpanzees (Pan troglodytes).

In addition to behavioral evaluations, stress assessments are also important for measuring animal welfare. Assessments of long-term stress are particularly important given that prolonged stress can affect physical health and reproduction. The use of hair cortisol as a marker of long-term stress has been increasing, but there has not yet been any report on the use of such methods with chimpanzees. Therefore, the purpose of this study was to establish and validate a methodology for analyzing hair cortisol in captive chimpanzees. In the first experiment, hair was removed from the arms of nine chimpanzees living in the Kumamoto Sanctuary (KS) and the regrown hair was sampled 3 months later. Fecal samples were collected periodically during the hair-growth period. The results showed that hair cortisol level was positively correlated with the rate of receiving aggression. Although the correlation between hair and fecal cortisol levels was not significant, the individual with the highest hair cortisol concentration also had the highest fecal cortisol concentration. These results suggest that hair cortisol may reflect long-term stress in chimpanzees. In the second experiment, we investigated the physiological factors affecting hair cortisol concentrations. We cut hair from the arms, sides, and backs of 25 chimpanzees living at the KS and the Primate Research Institute. The results revealed that cortisol varied based on source body part and hair whiteness. Therefore, we recommend that hair should always be collected from the same body part and that white hair should be avoided as much as possible.

Polymorphism of the tryptophan hydroxylase 2 (TPH2) gene is associated with chimpanzee neuroticism.

In the brain, serotonin production is controlled by tryptophan hydroxylase 2 (TPH2), a genotype. Previous studies found that mutations on the TPH2 locus in humans were associated with depression and studies of mice and studies of rhesus macaques have shown that the TPH2 locus was involved with aggressive behavior. We previously reported a functional single nucleotide polymorphism (SNP) in the form of an amino acid substitution, Q468R, in the chimpanzee TPH2 gene coding region. In the present study we tested whether this SNP was associated with neuroticism in captive and wild-born chimpanzees living in Japan and Guinea, respectively. Even after correcting for multiple tests (Bonferroni p = 0.05/6 = 0.008), Q468R was significantly related to higher neuroticism (ß = 0.372, p = 0.005). This study is the first to identify a genotype linked to a personality trait in chimpanzees. In light of the prior studies on humans, mice, and rhesus macaques, these findings suggest that the relationship between neuroticism and TPH2 has deep phylogenetic roots.

The first chimpanzee sanctuary in Japan: an attempt to care for the "surplus" of biomedical research.

This article specifically examines several aspects of the human-captive chimpanzee bond and the effort to create the first chimpanzee sanctuary in Japan. We discuss our ethical responsibility for captive chimpanzees that have been used in biomedical research. On April 1, 2007, the Chimpanzee Sanctuary Uto (CSU) was established as the first sanctuary for retired laboratory chimpanzees in Japan. This initiative was the result of the continuous efforts by members of Support for African/Asian Great Apes (SAGA), and the Great Ape Information Network to provide a solution to the large chimpanzee colony held in biomedical facilities. However, the cessation of invasive biomedical studies using chimpanzees has created a new set of challenges because Japan lacks registration and laws banning invasive ape experiments and lacks a national policy for the life-long care of retired laboratory chimpanzees. Therefore, CSU has initiated a relocation program in which 79 retired laboratory chimpanzees will be sent to domestic zoos and receive life-long care. By the end of 2009, the number of chimpanzees living at CSU had decreased from 79 to 59 individuals. A nationwide network of care facilities and CSU to provide life-long care of retired laboratory chimpanzees is growing across Japan. This will result in humane treatment of these research animals.

Diversification of bitter taste receptor gene family in western chimpanzees.

In mammals, bitter taste is mediated by T2R genes, which belong to the large family of seven transmembrane G protein-coupled receptors. Because T2Rs are directly involved in the interaction between mammals and their dietary sources, it is likely that these genes evolved to reflect species' specific diets during mammalian evolution. Here, we investigated the sequences of all 28 putative functional chimpanzee T2R genes (cT2Rs) in 46 western chimpanzees to compare the intraspecies variations in chimpanzees to those already known for all 25 human functional T2R genes (hT2Rs). The numbers of functional genes varied among individuals in western chimpanzees, and most chimpanzees had two or three more functional genes than humans. Similarly to hT2Rs, cT2Rs showed high nucleotide diversity along with a large number of amino acid substitutions. Comparison of the nucleotide substitution patterns in cT2Rs with those in five cT2R pseudogenes and 14 autosomal intergenic noncoding regions among the same individuals revealed that the evolution of cT2R genes was almost identical to that of putative neutral regions with slight but significantly positive Tajima's D values, suggesting that selective constraint on these genes was relaxed with weak balancing selection. These trends have resulted in the occurrence of various divergent alleles of T2Rs within the western chimpanzee populations and in heterozygous individuals who might have the ability to taste a broader range of substances.

Effects of early rearing conditions on problem-solving skill in captive male chimpanzees (Pan troglodytes).

Early rearing conditions of captive chimpanzees characterize behavioral differences in tool use, response to novelty, and sexual and maternal competence later in life. Restricted rearing conditions during early life hinder the acquisition and execution of such behaviors, which characterize the daily life of animals. This study examined whether rearing conditions affect adult male chimpanzees' behavior skills used for solving a problem with acquired locomotion behavior. Subjects were 13 male residents of the Chimpanzee Sanctuary Uto: 5 wild-born and 8 captive-born. A pretest assessed bed building and tool use abilities to verify behavioral differences between wild- and captive-born subjects, as earlier reports have described. Second, a banana-access test was conducted to investigate the problem-solving ability of climbing a bamboo pillar for accessing a banana, which might be the most efficient food access strategy for this setting. The test was repeated in a social setting. Results show that wild-born subjects were better able than captive-born subjects to use the provided materials for bed building and tool use. Results of the banana-access test show that wild-born subjects more frequently used a bamboo pillar for obtaining a banana with an efficient strategy than captive-born subjects did. Of the eight captive-born subjects, six avoided the bamboo pillars to get a banana and instead used, sometimes in a roundabout way, an iron pillar or fence. Results consistently underscored the adaptive and sophisticated skills of wild-born male chimpanzees in problem-solving tasks. The rearing conditions affected both the behavior acquisition and the execution of behaviors that had already been acquired.

How to crack nuts: acquisition process in captive chimpanzees (Pan troglodytes) observing a model.

Stone tool use for nut cracking consists of placing a hard-shelled nut onto a stone anvil and then cracking the shell open by pounding it with a stone hammer to get to the kernel. We investigated the acquisition of tool use for nut cracking in a group of captive chimpanzees to clarify what kind of understanding of the tools and actions will lead to the acquisition of this type of tool use in the presence of a skilled model. A human experimenter trained a male chimpanzee until he mastered the use of a hammer and anvil stone to crack open macadamia nuts. He was then put in a nut-cracking situation together with his group mates, who were naïve to this tool use; we did not have a control group without a model. The results showed that the process of acquisition could be broken down into several steps, including recognition of applying pressure to the nut,emergence of the use of a combination of three objects, emergence of the hitting action, using a tool for hitting, and hitting the nut. The chimpanzees recognized these different components separately and practiced them one after another. They gradually united these factors in their behavior leading to their first success. Their behavior did not clearly improve immediately after observing successful nut cracking by a peer, but observation of a skilled group member seemed to have a gradual, long-term influence on the acquisition of nut cracking by naïve chimpanzees.