Senile plaques and phosphorylated tau deposition in a super-aged rhesus monkey (Macaca mulatta).

The brain of a rhesus monkey that died at 43 years of age with symptoms of suspected cognitive dysfunction was analyzed. pathological analyses revealed characteristic Alzheimer's disease-related lesions: the aggregation of amyloid ß (Aß) in the form of senile plaques and phosphorylated tau proteins. We also revealed that Aß43, which is prone to aggregation and toxicity in humans, is involved in senile plaques in the brain of the rhesus monkey, as well as several other Aß species. Comparative studies of neuropathology using aged nonhuman primates lack behavioral descriptions compared to human medicine. This case report showed behavioral abnormalities and the detailed pathological changes that may have caused it in a super-aged rhesus monkey.

Reducing stress and stereotypic behaviors in captive female pygmy slow lorises (Nycticebus pygmeaus).

Improving captive conditions of pygmy slow lorises (Nekaris and Nijman have recently suggested that the pygmy slow loris should be called the pygmy loris and is distinctive enough to warrant a new genus, Xanthonycticebu) (Nycticebus pygmeaus) poses many challenges because detailed aspects of their lives in the wild are incomplete. This hinders efforts to replicate sustainable environments for them. To improve their well-being in captivity, eight rescued female pygmy slow lorises at the Japan Monkey Center (JMC) were socially housed in two types of groups following their solitary housing: two pairs and one group of four individuals. They spent much of their time in affiliative behaviors, as well as sharing sleeping sites after placement in a social group. The purpose of my study was to examine whether social housing helped in reducing stress by comparing fecal glucocorticoids and stereotypic behaviors when housed alone and when with conspecifics. Overall, the levels of fecal glucocorticoids were significantly lower when socially housed than when kept alone. One individual exhibited stereotypic behavior when housed alone, but this behavior disappeared after social housing. These findings support recent evidence that pygmy slow lorises are social animals and will benefit from group housing in captivity. We conclude that social housing of pygmy slow lorises improves their well-being by reducing stress levels, and that their group housing in captivity can provide dividends for the conservation of this endangered nocturnal primate because lorises intended for release should find it easier to adapt to natural conditions.

Hepatitis C virus infection reduces the lifespan of chimpanzees used in biomedical research.

Chimpanzees were used in hepatitis research for over three decades with the aim to identify and develop treatments for the virus, a leading cause of chronic liver disease in humans. We used a dataset of 120 chimpanzees housed at a single institution in Japan, 22 of whom became chronically infected with hepatitis C virus (HCV), to examine whether HCV infection results in a reduced lifespan as reported in humans. Survival analysis showed that HCV carriers experienced a higher mortality risk compared with non-carriers. Although no chimpanzee died from hepatic disease, carriers showed higher gamma-glutamyl transpeptidase (γGTP) levels compared with non-carriers suggesting that HCV infection negatively affected their liver condition. These results provide evidence that special attention is necessary to monitor the long-term condition of ex-biomedical primates.

Quantifying the 60-Year Contribution of Japanese Zoos and Aquariums to Peer-Reviewed Scientific Research.

With the shift in their social roles, modern zoos and aquariums are required to develop scientific research. Although zoos and aquariums worldwide have reported an increase in the number of papers they publish and the diversification of their fields in recent decades, the specific circumstances in Japan are slightly unclear. We listed peer-reviewed papers authored by Japanese zoos and aquariums using search engines and quantitatively evaluated the changes in the number of papers published over 62 years. Our results showed that papers published in Japan have increased remarkably since the 1990s, and research fields have diversified as in the rest of the world. In particular, joint research with research institutes has seen an upward trend, and the instances of English-language papers have increased. Meanwhile, the content of the research was biased. In zoos, research on animal welfare has been increasing, but the focus was heavily biased toward captive mammals. Aquariums contributed to the understanding of local ecosystems through the fundamental study of wildlife, but there were fewer papers on improving husbandry. Our results indicated that while research by Japanese zoos and aquariums is developing, research on welfare, conservation, and education regarding native endangered species must still be improved.

Do chimpanzees enjoy a virtual forest? A pilot investigation of the use of interactive art as a form of environmental enrichment for zoo-housed chimpanzees.

Environmental enrichment is essential for the well-being of zoo animals. Recent advances in sensor and video technologies may contribute to improvements in enrichment in terms of their flexibilities and time constraints. The purpose of this study was to investigate whether interactive movie art can be used as a form of environmental enrichment. We implemented interactive movies designed by a professional artist, a visual art aiming to reflect naturalistic forest habitat, in an indoor chimpanzee enclosure at Kyoto City Zoo in Japan. Motion-tracking sensors embedded in buoys were installed at several locations around the indoor enclosure; the chimpanzees could change the movie contents by physically interacting with these objects. We recorded behaviors by observing entire troop of chimpanzees (six) between March 16 and 20, 2020 (control condition), then recorded behaviors when the interactive movie was presented (experimental condition) between March 21 and 29, 2020. Behaviors were recorded via direct observations and video recordings to examine any changes after the installation of interactive art. The chimpanzees spent more time in the indoor enclosures during the experimental condition than during the control condition. Activity budgets did not change substantially during the study period. There was no evidence of habituation to the movie during the study period. Three chimpanzees, including two young chimpanzees, interacted with the movie more frequently than the others; these young chimpanzees occasionally showed playful expressions when interacting with the movie and exhibited different reactivities to the movie scenes. These results demonstrate, first, that the interactive art did not negatively affect chimpanzee behavior, and second, that some of the chimpanzees indeed showed positive responses to the art. This study, therefore, introduces a novel possibility for environmental enrichment in zoos, involving a collaboration between science and art.

Behavioral Changes of Solitary Housed Female Pygmy Slow Lorises (Nycticebus pygmeaus) after Introduction into Group Enclosures.

Pygmy slow lorises (Nycticebus pygmaeus) are threatened with extinction in the wild. Their nocturnal lifestyle and small size make them difficult to study in their natural habitat, but increasing evidence suggests that they are more social than previously thought. Our study was designed to assess the sociability of pygmy slow lorises by transferring six adult females from solo cages into environmentally enriched group home cages at the Japan Monkey Centre's Slow Loris Conservation Centre. Two females were paired to create one group, while the other four were placed together in a second group. We compared their social interactions, activity budgets, and postural behaviors before and after social housing was initiated. We found that all-female slow loris groups had a high degree of sociality, preferred to stay close to each other, nested together every night, and spent less time in locomotion and more time grooming than when living alone. These results suggest that female pygmy slow lorises actively seek companions when available. The captive housing of all-female groups of lorises could lead to better husbandry practices and improved animal welfare by allowing them to have conspecific companions. We conclude that isosexual groups of pygmy slow lorises should be preferred over single housing when possible.

Social relationships among captive male pygmy slow lorises (Nycticebus pygmaeus): Is forming male same-sex pairs a feasible management strategy?

Little is known about the social behavior of pygmy slow lorises, in particular, the social relationships of same-sex individuals have rarely been investigated. The Slow Loris Conservation Center was built at the Japan Monkey Center to enhance the welfare of confiscated slow lorises, promote their conservation, improve public education, and perform scientific research on the species. In the course of improving housing conditions, several same-sex pairs of pygmy slow lorises were formed. We monitored their behaviors and fecal glucocorticoid metabolite (FGM) levels to understand whether male same-sex pairings could be a feasible management strategy. The subjects were 10 male and 6 female lorises for comparison, all of whom were over 5 years old. We successfully formed five pairs of male lorises after eight formation attempts. Male pairs initially showed some aggressive behaviors; however, the rate decreased approximately 10 days after introduction. All of the male pairs eventually exhibited extensive affiliative social behaviors, including allogrooming and social play, during the dark (active) phase, and sleep site sharing during the light (inactive) phase. The rate of sleep site sharing during the light phase was higher than expected, suggesting that the pairs preferred to stay near each other. There was no evidence of increased stress after a long period of male-male social housing. Female same-sex pairs and male-female pairs demonstrated a high level of affiliative behaviors right after the introduction. These results highlight the flexibility and high sociability of this species and indicate that such same-sex pairings are a feasible option for their social management.

Development of bed-building behaviors in captive chimpanzees (Pan troglodytes): Implication for critical period hypothesis and captive management.

Wild great apes build beds for sleeping by combining tree branches or other vegetation, but the development of this behavior is poorly understood. We investigated the development of bed-building behaviors by conducting complementary cross-sectional and longitudinal studies of captive chimpanzees. In the cross-sectional study, we created an ethogram of behaviors related to bed-building by observing 59 chimpanzees living at the Kumamoto Sanctuary, Kyoto University, and the Kyoto City Zoo. In the longitudinal study, we installed bed-building platforms, provided branches on the platforms on a regular basis, and recorded behaviors of five chimpanzees (including an infant born in 2013) over a 3-year period from February 2015 to February 2018 at the Kyoto City Zoo (total 490.7 h). We found that all the chimpanzees performed some form of bed-building behavior but wild-born chimpanzees possessed more sophisticated techniques than captive-born chimpanzees. We also found that although the offspring of a wild-born female only showed simple techniques at the beginning of the longitudinal study, his repertoire of bed-building behaviors became as complex as that of his mother by the age of five. Our results suggest that improved bed-building behaviors can be supported in captive-born great apes by providing learning opportunities during appropriate stages of development.

Nighttime Suckling Behavior in Captive Giraffe (Giraffa camelopardalis reticulata).

Suckling behaviors are useful to better understand mother-offspring relationships. However, in many species, knowledge about nighttime suckling behavior is sparse. In the present study, we investigated suckling behavior in four calves of the reticulated giraffe (Giraffa camelopardalis reticulata) and their mother in the Kyoto City Zoo, Japan, by analyzing video clips of 9614 h. The relation between a calf's age and the mean duration and frequency of suckling were consistent with the results of previous daytime studies: the longest duration (80 ± 4 s) and highest frequency (0.41/h) of suckling occurred when the calves were young, and decreased thereafter. Suckling frequency was lower at night than during the day, probably because the mother spent much of the time resting at night. The mother initiated suckling behavior in offspring until six months of age. Most often, the mother terminated suckling except during the first few weeks after birth. Additionally, we reported that the average weaning period was 448 days (n = 5) and that the last born (sixth) continued to suckle for more than 750 days, which is a rare phenomenon. We believe the present report helps to fill the lack of knowledge about nighttime suckling behavior in giraffe.

Sleep-related behaviors in zoo-housed giraffes (Giraffa camelopardalis reticulata): Basic characteristics and effects of season and parturition.

Despite increasing interest in the behavior of zoo animals, studies of nocturnal behavior of zoo animals are limited. In this study, we investigated the relationship between parturition, season, and the sleep-related behaviors in captive reticulated giraffes to better understand the nocturnal life in giraffes. The subjects were two adult reticulated giraffes living in Kyoto City Zoo, Japan. Observations were made via an infrared camera that was mounted in the indoor enclosure between June 2007 and August 2009. We analyzed video clips that were recorded between 16:30 and 09:00 the next morning, over a total of 199 days. Sleep-related behaviors were classified into two categories based on the posture of the giraffes; recumbent posture and paradoxical sleep. We also recorded the laterality of recumbent posture, which was coded based on the direction of the legs against the torso (right or left). Seasonal differences in sleep behaviors between summer and winter were observed in both individuals. They tended to start to lie down earlier in the winter than in the summer. Parturition also affected the behaviors as both individuals decreased the behaviors before and after the parturition of the female. Additionally, the female lay on her left side less frequently than her right when resuming a recumbent posture in the pre-parturition period, while such laterality was not observed in the baseline and post-parturition period. These results suggested that season and parturition are important factors for determining the sleep-related behaviors in giraffes. Further studies are needed to understand how these changes in sleep affect other welfare parameters.

Common marmoset (Callithrix jacchus) personality, subjective well-being, hair cortisol level and AVPR1a, OPRM1, and DAT genotypes.

We studied personality, subjective well-being, and hair cortisol level, in common marmosets Callithrix jacchus, a small, cooperatively breeding New World monkey, by examining their associations with one another and genotypes. Subjects were 68 males and 9 females that lived in the RIKEN Center for Life Science Technologies. Personality and subjective well-being were assessed by keeper ratings on two questionnaires, hair samples were obtained to assay cortisol level and buccal swabs were used to assess AVPR1a, OPRM1 and DAT genotypes. Three personality domains-Dominance, Sociability, and Neuroticism-were identified. Consistent with findings in other species, Sociability and Neuroticism were related to higher and lower subjective well-being, respectively. Sociability was also associated with higher hair cortisol levels. The personality domains and hair cortisol levels were heritable and associated with genotypes: the short form of AVPR1a was associated with lower Neuroticism and the AA genotype of the A111T SNP of OPRM1 was related to lower Dominance, lower Neuroticism, and higher hair cortisol level. Some genetic associations were not in directions that one would expect given findings in other species. These findings provide insights into the proximate and ultimate bases of personality in common marmosets, other primates and humans.

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.

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.

Tools to tipple: ethanol ingestion by wild chimpanzees using leaf-sponges.

African apes and humans share a genetic mutation that enables them to effectively metabolize ethanol. However, voluntary ethanol consumption in this evolutionary radiation is documented only in modern humans. Here, we report evidence of the long-term and recurrent ingestion of ethanol from the raffia palm (Raphia hookeri, Arecaceae) by wild chimpanzees (Pan troglodytes verus) at Bossou in Guinea, West Africa, from 1995 to 2012. Chimpanzees at Bossou ingest this alcoholic beverage, often in large quantities, despite an average presence of ethanol of 3.1% alcohol by volume (ABV) and up to 6.9% ABV. Local people tap raffia palms and the sap collects in plastic containers, and chimpanzees use elementary technology-a leafy tool-to obtain this fermenting sap. These data show that ethanol does not act as a deterrent to feeding in this community of wild apes, supporting the idea that the last common ancestor of living African apes and modern humans was not averse to ingesting foods containing ethanol.

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.

Assessing the effects of cognitive experiments on the welfare of captive chimpanzees (Pan troglodytes) by direct comparison of activity budget between wild and captive chimpanzees.

We investigated the effects of cognitive experiments by direct comparison of activity budgets between wild and captive chimpanzees. One goal of captive management is to ensure that the activity budgets of captive animals are as similar as possible to those of their wild counterparts. However, such similarity has rarely been achieved. We compared the activity budget among three groups of chimpanzees: wild chimpanzees in Bossou (Guinea, n = 10), and captive chimpanzees who participated in cognitive experiments (experimental chimpanzees, n = 6) or did not participate in the experiments (nonexperimental chimpanzees, n = 6) at the Primate Research Institute (Japan). The experimental chimpanzees voluntarily participated in computer-controlled cognitive tasks and small pieces of fruits were provided as rewards. The data from captivity were obtained on the experimental days (weekdays) and nonexperimental days (weekends). In both study sites, we followed each chimpanzee from about 7 a.m. until the time when chimpanzees started to rest in the evening. The behaviors were recorded every 1 min. The results showed that on weekdays, feeding time and resting time of the experimental chimpanzees were almost the same as those of wild chimpanzees. However, for the nonexperimental chimpanzees, feeding time was significantly shorter and resting time was longer than those of the wild chimpanzees. In contrast, no difference was found in feeding time or resting time of the two groups of captive chimpanzees on weekends. The results suggested that the cognitive experiments worked as an efficient method for food-based enrichment.