Captive Japanese Macaques Research Articles

Housing relocation does not have to induce a significant stress response in captive Japanese macaques (Macaca fuscata).

Previous studies suggest that housing relocation may be stressful for captive non-human primates. Our study investigated the stress levels of Japanese macaques during a housing relocation by measuring their daily fecal cortisol metabolites, which are often used as an indicator of stress. Ten adult Japanese macaques, single-housed for research purposes, were relocated to a new facility. Fecal samples were collected daily for 7 days. Cortisol metabolite concentrations were determined via enzyme immunoassay. No significant differences in cortisol metabolite levels were found in 7 days, but concentration levels showed that the highest median was associated to the relocation day. The minimal cortisol metabolite increase suggests that there was a slight activity increase in the hypothalamic-pituitary-adrenal axis. Techniques encouraging cooperation of the monkeys, the short time duration of the relocation, and consistency in the environment may have contributed to the minimal stress levels observed.

In vitro digestion and fermentation of Japanese macaque (Macaca fuscata) food: The influence of food type and particle size.

Chewing is critical for herbivores to obtain nutrients. Measuring digesta particle size as the outcome of chewing can improve our understanding of the relationship between food and digestion. Previous studies of feeds of domestic animals have shown that smaller digesta particle size leads to more efficient digestion. Increased digesta particle size-either due to animal factors (e.g., a senile dentition) or to feed factors (e.g., fracture resistance) could be a sign of an animal experiencing compromised nutritional intake. However, for some primates that are dietary generalists, digesta particle size has been shown to increase when consuming preferred foods, which raises doubts about the role of chewing in digesting such foods. This uncertainty makes it difficult to understand the connection between diet, chewing, and digestion through digesta particle size in dietary generalists. In this study, using five typical food items from the Japanese macaque (Macaca fuscata) diet, we conducted in vitro digestibility and fermentation assays to explore the effects of particle size on enzymatic and microbial digestion. For the fermentation assays, we used feces from captive Japanese macaques as inoculum. Among the five food items, we found that particle size has a stronger influence on the digestibility of seeds and mature leaves compared to young leaves and pulp. The influence of particle size on the fermentation rate was stronger in pulp and seeds compared to that in leaves. The differences in physical structure, texture, digestion barriers, and soluble components may play important roles in such differences. These results support the hypothesis that reducing food particle size is less important for consuming fruits than for consuming leaves. The limited effects of particle size on digesting fruits suggest that the two fruits examined in this study are cost-effective concerning food processing and chewing.

Effects of short-term isolation on social animals' behavior: An experimental case study of Japanese macaque

One of the goals in animal socioecology is to understand the functions and dynamics of group living. While observations of free-ranging animals are a crucial source of information, an experimental investigation that manipulates the size or composition, or both, of animal groups in captivity can also bring complementary contributions to the research inquiry. When paired with an automatic data collection by biologging technology, experimental studies on captive animals also allow for big data analyses based on recent machine learning techniques. As an initial exploration of this research paradigm, the present study inquired to what extent isolation of captive Japanese macaques (Macaca fuscata) changed their movement patterns. Using three-dimensional location trajectories of the macaques that were systematically collected via Bluetooth Low Energy beacons and a deep neural network, we estimated the identifiability of whether a macaque was behaving in isolation or in group. We found that the neural network identified the isolation vs. in-group conditions with more than 90% accuracy from a five-minute location trajectory, suggesting that the isolation caused notable changes from the canonical group-living behaviors. In addition, the isolation made each individual more identifiable from one another based on their location trajectories.

Faecal proteomics as a novel method to study mammalian behaviour and physiology.

Mammalian faeces can be collected noninvasively during field research and provide valuable information on the ecology and evolution of the source individuals. Undigested food remains, genome/metagenome, steroid hormones, and stable isotopes obtained from faecal samples provide evidence on diet, host/symbiont genetics, and physiological status of the individuals. However, proteins in mammalian faeces have hardly been studied, which hinders the molecular investigations into the behaviour and physiology of the source individuals. Here, we apply mass spectrometry‐based proteomics to faecal samples (n = 10), collected from infant, juvenile, and adult captive Japanese macaques (Macaca fuscata), to describe the proteomes of the source individual, of the food it consumed, and its intestinal microbes. The results show that faecal proteomics is a useful method to: (i) investigate dietary changes along with breastfeeding and weaning, (ii) reveal the taxonomic and histological origin of the food items consumed, and (iii) estimate physiological status inside intestinal tracts. These types of insights are difficult or impossible to obtain through other molecular approaches. Most mammalian species are facing extinction risk and there is an urgent need to obtain knowledge on their ecology and evolution for better conservation strategy. The faecal proteomics framework we present here is easily applicable to wild settings and other mammalian species, and provides direct evidence of their behaviour and physiology.

Hematological and blood chemistry values in captive Japanese macaques (Macaca fuscata fuscata).

Biological information about captive Japanese macaques, including hematology and blood chemistry, is still lacking despite the fact that ethological and ecological data have accumulated during decades of field research. Hematological (511 examinations of 280 Japanese macaques) and blood chemistry data (between 33 and 284 examinations from between 29 and 257 individual macaques) in clinically healthy, simian retrovirus-free Japanese macaques tested between 2009 and 2013 were reviewed. Specific hematological and blood chemistry data for Japanese macaques without clinical signs of disease were provided in this study. Averages presented can be used as hematological parameters for Japanese macaques. Some differences between Japanese macaques and other closely related macaque species were found. Some parameters varied according to macaque age and sex, as well as regional origin. The data in this study will provide useful clinical indices for Japanese macaques in captive and similar conditions.

Improving the standards for gut microbiome analysis of fecal samples: insights from the field biology of Japanese macaques on Yakushima Island.

Fecal DNA-based 16S ribosomal RNA (rRNA) gene sequencing using next-generation sequencers allows us to understand the dynamic gut microbiome adaptation of animals to their specific habitats. Conventional techniques of fecal microbiome analysis have been developed within the broad contexts defined by human biology; hence, many of these techniques are not immediately applicable to wild nonhuman primates. In order to establish a standard experimental protocol for the analysis of the gut microbiomes of wild animals, we selected the Japanese macaques (Macaca fuscata yakui) on Yakushima Island. We tested different protocols for each stage of fecal sample processing: storage, DNA extraction, and choice of the sequencing region in the bacterial 16S rRNA gene. We also analyzed the gut microbiome of captive Japanese macaques as the control. The comparison of samples obtained from identical macaques but subjected to different protocols showed that the tested storage methods (RNAlater and lysis buffer) produced effectively the same composition of bacterial operational taxonomic units (OTUs) as the standard frozen storage method, although the relative abundance of each OTU was quantitatively affected. Taxonomic assignment of the detected bacterial groups was also significantly affected by the region being sequenced, indicating that sequencing regions and the corresponding polymerase chain reaction (PCR) primer pairs for the 16S rRNA gene should be carefully selected. This study improves the current standard methods for microbiome analysis in wild nonhuman primates. Japanese macaques were shown to be a suitable model for understanding microbiome adaptation to various environments.

Dix ans de collaboration entre la France et le Japon - Etudes sur la reproduction chez les macaques japonais

Our research interests are focused on the evolution of mating systems in primates and we aim at providing a better understanding of the adaptive signification of reproductive processes in female primates, using a comparative approach. Our Franco-Japanese collaboration (2006 - present) allowed us to study sociality and reproduction in a Catarrhine species, the Japanese macaque (Macaca fuscata), and on different but complementary topics (reproductive energetics, reproductive strategies, sexual signaling). We first investigated the links between energetics (i.e. nutritional status, body composition) and reproductive outcomes and our studies in captive Japanese macaques showed that, even in captivity with relaxed energetic constraints (e.g. constant food availability), seasonal breeding entails relatively high energy costs and females with higher energy status could invest more in reproductive activities and could afford to reproduce more rapidly. We also investigated the information that male Japanese macaques received from females that might enable them to discern periods with higher probabilities of conception and we developed a research program on the extent to which Japanese macaques, in common with people, have evolved a system of multimodal sexual signaling. We focused on the cues and signals available to males to make their mating decisions, and we provided information on the potential role of female behavior, female skin color, odours and vocalizations as sexual signals. We suggested, in particular, that females advertized their pregnancy through changes in behavioral, visual, and potentially auditory signals, and that males use these signals to adjust their mating behaviors and avoid wasting energy on non-reproductive copulations. This holistic study, combining fieldwork and laboratory experiments, and using a multidisciplinary approach (behavioral observations (sexual interactions), digital photography (visual scoring of female sexual skin color), hormonal (fecal ovarian steroids) and chemical data (components of female vaginal secretions)) allowed us to assess how different signals may combine to influence patterns of primate mate choices.

Genetic heterogeneity and phylogeny of Trichuris spp. from captive non-human primates based on ribosomal DNA sequence data

Nematodes of the genus Trichuris, known as whipworms, are recognized to infect numerous mammalian species including humans and non-human primates. Several Trichuris spp. have been described and species designation/identification is traditionally based on host-affiliation, although cross-infection and hybridization events may complicate species boundaries. The main aims of the present study were to genetically characterize adult Trichuris specimens from captive Japanese macaques (Macaca fuscata) and grivets (Chlorocebus aethiops), using the ribosomal DNA (ITS) as molecular marker and to investigate the phylogeny and the extent of genetic variation also by comparison with data on isolates from other humans, non-human primates and other hosts. The phylogenetic analysis of Trichuris sequences from M. fuscata and C. aethiops provided evidences of distinct clades and subclades thus advocating the existence of additional separated taxa. Neighbor Joining and Bayesian trees suggest that specimens from M. fuscata may be distinct from, but related to Trichuris trichiura, while a close relationship is suggested between the subclade formed by the specimens from C. aethiops and the subclade formed by T. suis.The tendency to associate Trichuris sp. to host species can lead to misleading taxonomic interpretations (i.e. whipworms found in primates are identified as T. trichiura). The results here obtained confirm previous evidences suggesting the existence of Trichuris spp. other than T. trichiura infecting non-human living primates.

Effects of seasonal changes in dietary energy on body weight of captive Japanese macaques (Macaca fuscata).

Food availability varies seasonally for wild animals, and body weight fluctuates accordingly in the wild. In contrast, controlling availability of diet under captive condition is difficult from keepers' standpoint, and monotonous diet often causes health problems in captive animals. We evaluated the effects of a seasonally controlled diet on body weight of captive Japanese macaques (Macaca fuscata) in an outside enclosure at Ueno Zoo, Tokyo, Japan. We fed a high-energy diet in spring and fall, and a more restricted diet in summer and winter for 3 years (2011-2013). Seasonal changes in body weight were similar to those that occur in wild macaques: for both sexes, body weight was higher in spring and fall and lower in winter. A decrease in body weight between fall and winter occurred only in adults, which implied that reducing dietary intake in winter had a more severe effect on adults than on juveniles. Different from wild populations, the body weight of captive macaques did not decrease between spring and summer, which we attributed to a lack of movement within the enclosure and to excess energy intake in summer. In addition to controlling dietary composition, providing large enclosure with complex structure and making efforts of giving unpredictability in feeding are necessary to motivate the captive animals to be more active, which would cause the macaques to show seasonal change in body weight, which is found in wild.

Environmental, biological, and social factors influencing fecal adrenal steroid concentrations in female Japanese macaques (Macaca fuscata).

The ability to determine hormonal profiles of primate populations using non-invasive techniques can help to monitor physical fitness, stress, and physiological responses to environmental changes. We investigated fecal glucocorticoids (fGC) and DHEAS concentrations in captive Japanese macaques (Macaca fuscata) in relation to environmental, biological, and social factors. The subjects were female Japanese monkeys from 4 months to 31 years old housed in captivity (27 in social groups and 12 in single cages). Fecal samples were collected from all females, and behavioral data from the social groups during the mating season and the following birth season. Hormonal concentrations were analyzed by enzyme immunoassay. Our results revealed that both fGC and fecal DHEAS concentrations are higher in females housed indoors in single cages than in those living outdoors in social groups. We also found that fGC concentrations were higher in the cycling females during the mating (winter) season than the lactating females in the birth (spring) season. Age was negatively associated to both fGC and fecal DHEAS levels, but the relationship between age and fecal DHEAS was more evident in females housed indoors in single cages than in females housed in outdoor social groups. We did not observe any association of dominance rank with either fecal DHEAS or fGC. This study showed that measurement of fecal DHEAS and fGC can be a good method to assess stress in Japanese macaques. These findings provide insights about the physiology of these two adrenal hormones in female Japanese macaques, which can be applied to wild populations and is fundamental for captive management and conservation biology.

Seroprevalence of Japanese encephalitis virus infection in captive Japanese macaques (Macaca fuscata).

Japanese encephalitis virus (JEV), which is transmitted by mosquitoes, infects many animal species and causes serious acute encephalitis in humans and horses. In this study, a serosurvey of JEV in Japanese macaques (Macaca fuscata) reared in Aichi Prefecture was conducted using purified JEV as an antigen for ELISA. The results revealed that 146 of 332 monkeys (44%) were seropositive for JEV. In addition, 35 of 131 monkeys (27%) born in the facility were seropositive, and the annual infection rate in the facility was estimated as 13%. Our results provide evidence of the frequent exposure of many Japanese macaques to JEV, suggesting that there is a risk of JEV transmission to humans by mosquitoes.

Japanese monkeys (Macaca fuscata) spontaneously associate alarm calls with snakes appearing in the left visual field.

Many socially living animals are sensitive to a potential predator as part of their antipredator strategy. Alarm calls function to deter predators and to help other group members detect danger. The left visual field is involved in detection of potential threats or predators in many vertebrates, but it is unclear how alarm calls influence visual detection of a potential predator. Here, we experimentally examined how alarm calls spontaneously influence the search for pictures of a potential predator in captive Japanese macaques. We used an audiovisual preferential-looking paradigm by presenting pictures of a snake and a flower simultaneous with either a recording of alarm calls or contact calls. We found no difference in gaze duration between the 2 picture types when playing back contact calls. Monkeys looked significantly longer at pictures of snakes than at those of flowers when alarm calls were played back if the snake pictures were presented on the left side of the monkey's visual field, indicating right hemispheric bias during processing of predator representations. This is the first laboratory demonstration of auditory enhancement of visual detection of predators in the left visual field in animals, which will contribute to a better understanding of alarm call studies conducted in the wild.

飼育下ニホンザルにおけるα個体の推移

飼育下ニホンザルにおけるα個体の推移

Erratum to: Characteristics of stable isotope signature of diet in tissues of captive Japanese macaques as revealed by controlled feeding

Erratum to: Characteristics of stable isotope signature of diet in tissues of captive Japanese macaques as revealed by controlled feeding

The influence of age and season on fecal dehydroepiandrosterone-sulfate (DHEAS) concentrations in Japanese macaques (Macaca fuscata)

Dehydroepiandrosterone (DHEA) and its sulfate, DHEAS, are the most abundant steroid hormones in primates, providing a large reservoir of precursors for the production of androgens. DHEAS levels decline with age in adult humans and nonhuman primates, prompting its consideration as a biomarker of senescence. However, the mechanisms responsible for this age-related decrease and its relationship to reproduction remain elusive. This research investigated DHEAS concentrations in fecal samples in order to determine age-related changes in captive Japanese macaques, as well as to assess the possible influence of seasonality. The subjects were 25 female Japanese macaques (2weeks to 14years-old) housed outdoors in social groups at the Primate Research Institute. We collected three fecal samples from each animal during the breeding season (October to December) and three additional samples from adult females during the non-breeding season (May to June). The hormonal concentrations were determined using enzyme immunoassay. DHEAS concentration was negatively correlated with age, but we did not find a significant difference between breeding and non-breeding seasons. Neonatal macaques had the highest DHEAS concentrations of all age groups. We suggest that elevated neonatal DHEAS is possibly a residue from fetal adrenal secretion and that, as in humans, it might assist in neurobiological development.

Characteristics of stable isotope signature of diet in tissues of captive Japanese macaques as revealed by controlled feeding

We determined the magnitude of isotopic fractionation of carbon and nitrogen stable isotope ratios (as enrichment factors, Δδ(13)C and Δδ(15)N, respectively) between the tissues and diets of captive Japanese macaques (Macaca fuscata) using a controlled feeding experiment, to provide basic data for reconstructing their feeding habits. The Δδ(13)C and Δδ(15)N values, respectively, were 0.9 ± 0.2 ‰ (mean ± standard deviation, SD) and 3.0 ± 0.3 ‰ for whole blood, 1.3 ± 0.2 ‰ and 4.3 ± 0.3 ‰ for plasma, and 0.8 ± 0.2 ‰ and 3.0 ± 0.2 ‰ for red blood cells. However, the Δδ(13)C and Δδ(15)N values for hair were 2.8 ± 0.3 ‰ and 3.4 ± 0.2 ‰, respectively. No difference was detected in the δ(13)C and δ(15)N values of hair sampled from different parts of the body. We investigated the effects of diet on δ(13)C in growing hair by alternating the diet of the macaques each month between two diets that differed markedly in δ(13)C. Hair regrown after shaving repeatedly recorded the δ(13)C of the diet consumed during the time of hair growth. On the other hand, hair naturally grown during the diet-change experiment did not show a clear pattern. One possible reason is that the hair had grown abnormally under unnatural indoor conditions and showed complicated isotope signatures. To reconstruct the long-term feeding history of Japanese macaques, we need to further clarify the relationships between the stable isotope signature of diet and various body tissues.

Tetanus as Cause of Mass Die-off of Captive Japanese Macaques, Japan, 2008

In 2008 in Japan, 15/60 captive Japanese macaques died. Clostridium tetani was isolated from 1 monkey, and 11 had tetanus-specific symptoms. We conclude the outbreak resulted from severe environmental C. tetani contamination. Similar outbreaks could be prevented by vaccinating all monkeys, disinfecting housing areas/play equipment, replacing highly C. tetani–contaminated soil, and conducting epidemiologic surveys.

Use of video system and its effects on abnormal behaviour in captive Japanese macaques (Macaca fuscata)

Although nonhuman primates have highly developed visual cognitive abilities, they have few opportunities to exert such abilities in captivity. Video presentation can reproduce multiple features of the complex, real, visual world. Therefore, video presentation can be expected to act as environmental enrichment for captive primates. The present study evaluated the enriching effects of novelty and content of videos as well as control over videos using newly developed technology including network-shared YouTube videos and an infrared distance sensor. Baseline data were obtained for 10 days without video display and then 10 days with the display showing no videos in four individually housed monkeys and six pair-housed monkeys. The monkeys were then exposed to videos of conspecifics, people, and animation and observed for 30 days. In some days, the monkeys had control over videos such that videos played only when subjects sat directly in front of the display. Observations were then taken for an additional 10 days with no videos. Behaviours such as time watching videos, abnormal behaviour and time spent in front of display were recorded for 60min per day using instantaneous sampling with a 30-s interval. Monkeys displayed fewer abnormal behaviours when the video was playing (individually housed: 11.3 sampling points, pair-housed: 7.7 sampling points) than when the video was not playing (individual housed: 22.5 sampling points, pair-housed: 10.8 sampling points) (P<0.001). The abnormal behaviour over the course of the observation days showed no evidence of habituation to videos. The frequency of watching the videos and abnormal behaviour differed depending on the presented contents of videos (P<0.001). The subjects spent more time in front of the display in the days in which they could control the videos (individually housed: 89.1 sampling points, pair-housed: 17.6 sampling points) than in those in which they had no control (individually housed: 70.1 sampling points, pair-housed: 7.3 sampling points) (P<0.001), suggesting that they were preferentially choosing to watch the videos. These results suggest that video presentation can be a useful technique to decrease abnormal behaviour of captive Japanese macaques. The content and controllability over videos were influential on their behaviour, suggesting that implementation of video enrichment that includes conspecifics videos and controllability over videos can improve animal welfare. Implementation based on an understanding of species-specific characteristics can contribute to effective environmental enrichment.

動画呈示によるケージ飼育ニホンザルの異常行動の軽減と新奇性・内容・操作性の効果

動画呈示によるケージ飼育ニホンザルの異常行動の軽減と新奇性・内容・操作性の効果

Age class differences in the feeding behavior of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups

Age class differences in feeding behavior of primates are affected by many factors, including feeding competition, foraging skills, habitat type, food abundance and distribution, body mass, and food types. Two captive groups of Japanese macaques (Macaca fuscata), one housed in a forested enclosure and the other in a nonvegetated enclosure, were studied to examine the effect of environmental enrichment on age class differences in feeding behavior. Although there was no significant age class difference in time spent feeding on provisioned foods in either enclosure, the feeding rate (intake of unit food/minute) of adults consuming provisioned monkey chow was significantly higher than that of immatures in both enclosures, and was faster for both age groups in the nonvegetated than in the forested enclosure. Overall, feeding time was greatly extended for individuals of both age classes in the forested enclosure compared with their counterparts in the nonvegetated enclosure. Immatures in the forested enclosure utilized a significantly greater number of plant species and food items, exploiting many food items available among the terminal branches, and spent significantly more time feeding than adults. Perhaps constrained by larger body size, adults fed more often on the ground or middle height of the trees, likely reducing competition over plant food resources between adults and immatures. The natural vegetation played an important role in extending feeding time and segregating substrate use during feeding by adults and immatures. This study revealed the benefits concerning environmental enrichment of a naturally forested enclosure, which provides captive primates the opportunity to exhibit age class and species-typical feeding behaviors of importance for their dietary maintenance and general health.