Captive Japanese Macaques Research Articles

GENETIC CHARACTERISTICS AND ANTIMICROBIAL RESISTANCE OF ESCHERICHIA COLI FROM JAPANESE MACAQUES (MACACA FUSCATA) IN RURAL JAPAN

Escherichia coli was isolated from wild and captive Japanese macaques (Macaca fuscata) to investigate the risk of zoonotic infections and the prevalence of antimicrobial-resistant Escherichia coli in the wild macaque population in Shimokita Peninsula, a rural area of Japan. We collected 265 fresh fecal samples from wild macaques and 20 samples from captive macaques in 2005 and 2006 for E. coli isolation. The predominant isolates were characterized by serotyping, virulence gene profiling, plasmid profiling, pulsed-field gel electrophoresis (PFGE), and microbial sensitivity tests. In total, 248 E. coli strains were isolated from 159 fecal samples from wild macaques, and 42 E. coli were isolated from 17 samples from captive macaques. None of the virulence genes eae, stx, elt, and est were detected in any of the isolates. The relatedness between wild- and captive-derived isolates was low by serotyping, PFGE, and plasmid profiling. Serotypes O8:H6, O8:H34, O8:H42, O8:HUT, O103:H27, O103:HNM, and OUT:H27 were found in wild macaque feces; serotypes O157:H42 and O119:H21 were recovered from captive macaques. O-and H-serotypes of the 26 isolates were not typed by commercial typing antisera and were named OUT and HUT, respectively. Twenty-eight isolates had no flagellar antigen, and their H-serotypes were named HNM. Similarity of PFGE patterns between wild-derived isolates and captive-derived isolates was <70%. No plasmid profile was shared between wild-derived and captive-derived isolates. The prevalence of antimicrobial-resistant E. coli was 6.5% (n=62) in wild macaques, and these isolates were resistant to cephalothin. We conclude that wild Japanese macaques in Shimokita Peninsula were unlikely to act as a reservoir of pathogenic E. coli for humans and that antimicrobial-resistant E. coli in wild macaques may be derived from humans.

Digesta Passage Time, Digestibility, and Total Gut Fill in Captive Japanese Macaques (Macaca fuscata): Effects Food Type and Food Intake Level

Digestion is an important process in understanding the feeding ecology of animals. We examined digesta passage time, digestibility, and total gut fill in Japanese macaques (Macaca fuscata; n = 4) under 4 dietary conditions representing the seasonal and regional variations in the diets of wild populations to determine the effects of food type and food intake on these digestive features. Food type is associated with mean retention time (MRT), digestibility, and total gut fill. Dry matter intake (DMI) of food correlates positively with total gut fill but not with MRT or digestibility. Conversely, indigestible DMI affected MRT negatively. Thus, when Japanese macaques consume high-fiber foods, MRT becomes shorter and digestibility is lower than when eating low-fiber foods. Moreover, macaques experience increases in total gut fill when they consume high-fiber diets or a large amount of food. Japanese macaques may excrete difficult-to-digest food components quickly; they nevertheless buffer an increase in food intake by an increase in gut fill. Our study offers new insights into the relationship between feeding ecology and nutritional physiology in primates by simultaneously examining the effects of food type and intake level on MRT and digestibility.

Effects of the physical characteristics of seeds on gastrointestinal passage time in captive Japanese macaques

The time it takes seeds to pass through the gut of vertebrates is an important aspect of endozoochorous seed dispersal because it influences seed dispersal distance. The physical characteristics of seeds (e.g. dry seed weight, volume and specific gravity) vary among plant species, which might cause a difference in seed movement through the gastrointestinal system. We conducted feeding experiments with captive female Japanese macaques Macaca fuscata (n=5) using eight different types of seeds to evaluate the effects of the physical characteristics of seeds on their passage time. The median seed recovery percentage for the real seeds was 35.5% (range, 24–78%). Among three passage time variables examined, the mean retention time (MRT) (37–54 h) and time of last appearance of a seed (TLA) (53–109 h) differed significantly among seed types, and the former differed significantly among individuals. Transit time (TT) (22–35 h) did not. The generalized linear models (GLM) selected dry seed weight as the most important factor affecting MRT, and specific gravity of seeds as the most important factor affecting TLA. This implies that (1) heavier seeds and (or) seeds with greater specific gravity remain in the gut longer and are likely to be dispersed farther from the parent plant; (2) the lighter seeds and (or) seeds with lower specific gravity are dispersed nearer the parent. Our study demonstrated the importance of considering the effects of the physical characteristics of seeds on the manner in which primates disperse plant species, although we should consider the effect of the individual variation in the passage time, too.

Seasonal and reproductive variation in body condition in captive female Japanese macaques (Macaca fuscata)

The geographic distribution of Japanese macaques includes populations with the most northern range of any primate species. Not surprisingly, females of this species are characterized by physiological adaptations and unique fat deposition mechanisms that facilitate their survival through the sometimes-harsh seasonal conditions of temperate climates, as well as sustaining the metabolic costs of mating, pregnancy, and lactation. Here, we explore the relationship between nutritional status, seasonality, and reproductive status using anthropometric and leptin measures from 14 captive female Japanese macaques. No seasonal patterns were found in the levels of leptin, but there were differences between seasons in anthropometric measures, specifically between the beginning and the end of the mating season. Females gained weight and accumulated energy reserves in fall to prepare for mating activity, and to survive the severe conditions of winter, which is also the period of gestation if pregnancy occurs. Lactating females had larger total skinfolds relative to nonlactating individuals, and females with older babies at the beginning of the mating season had larger abdominal skinfolds than did those with younger babies. There was a relationship between the likelihood of conception and nutritional status, with females that conceived during one mating season being in better condition at the end of their previous mating season. Together, these results suggest that, even in captive settings, seasonal breeding has a cost on the energetic demands of mating, and that higher condition (i.e. fatter) females could afford the demands of lactation and reproduced more rapidly.

Isolation and characterization of a potentially virulent speciesEntamoeba nuttallifrom captive Japanese macaques

We have recently proposed revival of the name Entamoeba nuttalli Castellani, 1908 for a virulent amoeba (P19-061405 strain) isolated from a rhesus monkey (Macaca mulatta) and located phylogenetically between E. histolytica and E. dispar. In this study, E. nuttalli was isolated from feces of captive Japanese macaques (M. fuscata) in an open-air corral in Japan. The sequence of the 18S rRNA gene in the isolates differed from the P19-061405 strain in 2 nucleotide positions, but was identical to the EHMfas1 strain isolated previously from a cynomolgus monkey (M. fascicularis). One of the E. nuttalli isolates from Japanese macaques, named the NASA6 strain, was axenized and cloned. In isoenzyme analysis, the mobilities of hexokinase and phosphate glucose isomerase in the NASA6 strain were identical to those in the P19-061405 and EHMfas1 strains, but the mobility of phosphoglucomutase was different. These results were supported by gene analyses of these enzymes. Inoculation of NASA6 strain trophozoites into the liver of hamsters led to formation of an amoebic liver abscess. The liver lesions were characterized by extensive necrosis associated with inflammatory reactions. These results demonstrate that the NASA6 strain is potentially virulent and that E. nuttalli should be recognized as a common parasite in macaques.

尿および糞を用いたサル類の非侵襲的ホルモン測定法とその応用―Ｆｉｅｌｄ Ｅｎｄｏｃｒｉｎｏｌｏｇｙのすすめ―

Noninvasive methods for the measurement of estrone conjugates (E1C), pregnanediol-3-glucronide (PdG), testosterone (T), follicle stimulating hormone (FSH), monkey chorionic gonadotropin (mCG) and cortisol in excreta of non-human primates were described. In the series of studies, results suggest that 1) urinary and fecal steroid metabolites accurately reflected the same ovarian or testicular events as observed in plasma steroid profiles in captive Japanese macaques, time lags associated with fecal measurements were one day after appearance in urine; 2) these noninvasive methods were applicable to wild and free-ranging animals for determining reproductive status; 3) hormonal changes during menstrual cycles and pregnancy could be analyzed by measurement of FSH, CG and steroid metabolites in the excreta in captive great apes and macaques; and 4) hormone-behavior relationships of macaques in their natural habitats and social setting could be analyzed. In these studies, we confirmed an association between maternal rejection and excreted estrogen, but not excreted progesterone, for Japanese macaques. We also reported that significantly higher levels of fecal cortisol were observed in high-ranking male Japanese macaques. 5) A reliable non- instrumented enzyme-linked immunosorbent assay for detection of early pregnancy in macaques was established.These results suggest that the noninvasive methods for monitoring characteristics of excreted hormones provide a stress-free approach to the accurate evaluation of reproductive status in primates. These methods provide the opportunities for the study of hormone-behavior interactions in not only captive but also wild and free-ranging animal species.

Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata)

Individuals adapt to changes in their environment, such as food availability and temperature, by adjusting the amount of time spent in different behavioral activities. These adjustments in behavior should vary across age-sex class according to specific physiological and social needs. We studied the activity budgets of three social Japanese macaque groups inhabiting either vegetated or nonvegetated enclosures in order to compare the effects of access with vegetation, as both food and substrate on resting, feeding, grooming and moving activities over a 12-month period. Daily access to natural foods for monkeys in the vegetated enclosure seems to be largely responsible for the differences in daily time budgets of these three groups. Resting time in all three groups was longer than the time devoted to other activities. Resting and moving time in the two nonvegetated enclosures was significantly longer than in the vegetated enclosure. In contrast, feeding and grooming time was significantly longer in the vegetated enclosure. Seasonal variation in time spent feeding, resting and grooming was significantly effected by enclosure type. In all three enclosures, immatures, particularly females, spent more time feeding and moving, whereas adults spent more time resting. Significant monthly variation in time spent by age-sex class was noted only for feeding and resting. Interestingly, in the vegetated enclosure, time spent feeding on natural vegetation was equal to the amount of time spent feeding on provisioned food. This suggests that factors other than energetic and nutritional needs may be important determinants of the activity budget of the species. These results have important implications for the enrichment of captive primates and our understanding of the maintenance of activity patterns by primates in the wild.

Comparison of activity budgets of captive Japanese macaques (Macaca fuscata) in two different enclosure environments

Comparison of activity budgets of captive Japanese macaques (Macaca fuscata) in two different enclosure environments

Grooming and aggression in captive Japanese macaques

This study investigated the relations between allogrooming and aggression in a captive group of Japanese macaques (Macaca fuscata). Our aim was to test whether evidence of an interchange between allogrooming and a reduction in aggression could be identified at a group level. Female Japanese macaques did not direct less aggression to those group mates that groomed them most. Although generally they did not direct more grooming to those group mates that attacked them most, they did show increased grooming towards those nonkin group mates that showed the most aggression. These results are interpreted in light of the conflicting processes that are likely to underlie macaque social choices.

Studies on Reproductive Endocrinology in Non-human Primates: Application of Non-invasive Methods

A practical method for the quantitative measurement of estrone conjugates (E1C), pregnanediol-3-glucronide (PdG), follicle stimulating hormone (FSH), and monkey chorionic gonadotropin (mCG) in the excreta of non-human primates were described. In the series of studies, results suggest that 1) urinary and fecal steroid metabolites accurately reflected the same ovarian or testicular events as observed in plasma steroid profiles in captive Japanese macaques, time lags associated with fecal measurements were one day after appearance in urine; 2) these noninvasive methods were applicable to wild and free-ranging macaques for determining reproductive status; 3) hormonal changes during menstrual cycles and pregnancy could be analyzed by measurement of FSH, CG and steroid metabolites in the excreta in captive great apes and macaques; and 4) hormone-behavior relationships of macaques in their natural habitats and social setting could be analyzed. In macaques, between maternal rejection and excreted estrogen, but not excreted progesterone were associated, moreover, in male study, significantly higher levels of fecal cortisol were observed in high-ranking males. In addition, reliable noninstrumented enzyme-linked immunosorbent assay (NELISA) for detection of early pregnancy in macaques was established. These results suggest that the noninvasive characteristic of excreted hormone monitoring provide a stress-free approach to the accurate evaluation of reproductive status in primates.

Variability in behavior frequencies and consistency in transactions across seasons in captive Japanese macaques (Macaca fuscata)

AbstractConsistent interspecific differences are found in macaque species, ranging from highly hierarchical and nepotistic societies to more tolerant and open social organizations. It still remains to be demonstrated whether intraspecific variation is narrower than interspecific variation. Herein, we quantified social behavior in a captive group of Japanese macaques (Macaca fuscata) to estimate the range of intraspecific variation for a full array of measurements in three different seasons. Despite an increased frequency of aggression found on the part of males during the mating season, the form of the behaviors performed remained relatively unchanged. Transactions during conflicts, approaches, or grooming did not undergo significant variations in relation to season. Frequencies and durations seemed more sensitive to demographic and environmental variations. The values measured in the study group are representative of the Japanese macaque. The results validate the use of transaction measurements in interspecific comparisons, providing that additional factors such as age and sex are taken into account. Aggr. Behav. 29:81–93, 2003. © 2003 Wiley‐Liss, Inc.

Measurement of urinary and fecal steroid metabolites during the ovarian cycle in captive and wild Japanese macaques, Macaca fuscata.

We measured the concentration of steroid hormones from urine, feces, and blood samples of two captive Japanese macaques, Macaca fuscata, during nonconceptive ovarian cycles to compare the patterns of the excreted steroids with those of circulating steroids. Urine and feces were analyzed for estrone conjugates (E1C) and pregnanediol-3-glucronide (PdG) using enzyme immunoassays (EIAs), while plasma was analyzed for estradiol-17beta(E2), progesterone (P), and luteinizing hormone (LH) using radioimmunoassays (RIAs). Urinary and fecal E1C and PdG levels were approximately parallel to plasma E2 and P levels, respectively. The E1C profiles of daily urinary and fecal samples revealed a midcycle peak, followed by a sustained PdG increase lasting up to two weeks from the E1C peak. A fecal E1C peak was one day later than the urinary E1C peak. One of the captive females exhibited a discrete plasma LH peak, one indicator that ovulation has occurred, on the day following the urinary E1C peak, i.e., the same day of fecal E1C peak. We measured excreted steroids in nine wild females and determined the timing of ovulation by comparing fecal steroid profiles to those obtained in captive monkeys. Data from wild females indicated that eight of nine females conceived during their first ovulatory cycle of the sampling period, whereas the remaining female failed to conceive during the sampling period even though she ovulated. In the eight females that conceived, E1C increased again following the detected or estimated E1C peak, with levels comparable to the preovulatory peak levels, and sustained elevations of PdG for over 40 days. These data illustrate that the urinary and fecal profiles of ovarian steroid excretion obtained through the application of these noninvasive techniques provide an accurate approach for monitoring conceptive and nonconceptive ovarian cycle in captive and free-living Japanese macaques.

The influence of rearing conditions on the physical growth of captive Japanese macaques (Macaca fuscata).

To clarify the influence of rearing conditions on the growth of various body parts of Japanese macaques (Macaca fuscata), two groups reared under different conditions, i.e., a group born and reared in open enclosures (Enclosure group) and another consisting of macaques born and reared in cages (Caged group), were somatometrically analyzed. Somatometric data on 36 measures of various body parts were collected from 77 males and 92 females. Growth in many body parts was smaller in the Caged group than in the Enclosure group. Body parts that exhibited large incremental increases were more sensitive to differences in rearing space at the infantile growth stage in both sexes. Recovery from delayed growth at the pubertal growth stage was found in many body parts. However, the size of some locomotor elements such as the wrist and hand, and ankle and foot strongly reflected limitations of space and changes due to this were irreversible. Females were more sensitive than males to such differences in rearing conditions. We conclude that open enclosures with ample rearing space are necessary for the innate growth of Japanese macaques to occur.

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans.

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.

Mother-infant conflict over behavioral thermoregulation in Japanese macaques

This study evaluated the effects of time of day, ambient temperature, and relative humidity on mother-infant interactions in captive Japanese macaques (Macaca fuscata). Unlike time of day and relative humidity, temperature influenced mother-infant interactions. Even though total time spent in ventroventral contact did not change, lower temperatures were associated with greater attempts by the infants to maintain contact with their mothers and with more frequent maternal rejection. Effects of temperature on mother-infant interactions were not mediated by the effects of temperature on mothers' general activity. These results are interpreted in light of the different thermoregulatory needs of mothers and infants, and highlight a previously neglected cause for mother-infant conflict.

Intragroup Variation in Conciliatory Tendencies in Captive Japanese Macaques

Nonhuman primates have been observed to exchange friendly gestures soon after an agonistic episode, a behaviour labelled reconciliation. Frequency of reconciliation has been shown to vary both within and between primate groups. This study used both univariate and multivariate analyses to investigate intragroup variation in the frequency of reconciliation in captive Japanese macaques (Macaca fuscata). Frequency of reconciliation was lower during the mating season, and was also affected by the intensity of aggression and by the sex and age combination of the opponents. On the contrary, outcome of aggression and number of aggressors did not influence the frequency of reconciliation. Kin reconciled more than nonkin, and individuals with a good social relationship reconciled more than those with a bad or weak relationship. The effects of kinship and relationship quality appeared to be independent since among individuals with a good relationship, kin reconciled more than nonkin, while among nonkin, individuals with a good relationship reconciled more than those with a bad or weak relationship. Our results show that Japanese macaques are highly flexible in their conciliatory behaviour, and highlight a possible role of reconciliation in the negotiation and management of primate social relationships.

Group composition affects seasonal birth timing in captive Japanese macaques

We analyzed birth dates recorded during an 18-year period in a group of Japanese macaques housed in the Rome zoo to assess the influence of environmental, physiological, and social factors on birth seasonality. Birth timing differed significantly among years. Birth timing was affected by reproductive condition of females—ones that had given birth in the previous year delivered significantly later than those that had not—but not by their age or dominance rank. We conducted further analyses separately on females that had or had not given birth in the previous year. In both subgroups of females mean birth date was not influenced either by environmental temperature and rainfall during the previous mating season or by group size. On the contrary, among females that had not given birth in the previous year, socionomic sex ratio—ratio of sexually mature males to sexually mature females—is positively correlated with both mean birth date and date of the first birth, but not with date of the last birth. Contrarily, among females that had given birth in the previous year, there is no significant relationship between these variables. We hypothesize that the effects of socionomic sex ratio on birth timing might depend on competition among males for access to fertile females. When the number of males per female was higher, mutual disruption of consort pairs may have led to a delay in the onset of mating.

Kinship bonds are not necessary for maintaining matrilineal rank in captive Japanese macaques

Although kinship is of central importance in matrilineal (nepotistic) dominance systems, various lines of evidence indicate that its role has probably been overestimated. For example, alliances among nonkin, patterned on the basis of dominance per se, contribute to the maintenance of rank and to the remarkable stability of matrilineal rank orders. But because kin and nonkin alliances exert their stabilizing effects on the rank order simultaneously, the effect of nonkin alliances per se is unknown. We tested whether nonkin alliances are sufficient to ensure the stability of matrilineal rank relations in a laboratory-housed group of Japanese macaques (Macaca fuscata). We first created a group composed of two female subgroups: (1) a subordinate subgroup of close kin known to constitute an effective revolutionary alliance and (2) a dominant subgroup composed mostly of nonkin and distant kin known to support each other against lower-ranking females. In the course of 12 consecutive experimental manipulations, we reduced progressively the relative power of the dominant subgroup by manipulating its size and age composition. The members of the dominant subgroup maintained their rank in all experimental situations except when alone. Thus, nonkin alliances remained effective up to extremely pronounced levels of power imbalance. These results suggest that the remarkable stability of matrilineal rank orders is not conditional upon the existence of nepotistic alliances and strong matrilines of close kin.

Variations in fundamental frequency peak position in Japanese macaque (Macaca fuscata) coo calls.

Japanese macaques (Macaca fuscata) produce coo calls whose use in various contexts is correlated with differences in the relative temporal position of the peak value of a call's fundamental frequency (Green, 1975). Studies have produced conflicting results about both the location of the category boundary between smooth early high and smooth late high coo subtypes and macaques' perceptual sensitivity to variations in peak position. In this study, fundamental frequency peak positions were measured in 578 coos produced by 8 captive adult female Japanese macaques in order to test whether calls with peak positions close to either of 2 hypothesized boundaries occurred at low rates. Overall, such calls were found to occur at rate equal to or higher than predicted by chance. Peak position varied more consistently between animals than by behavioral context. The results may indicate that peak position in coos does not form 2 distinct categories.

Development of mother‐infant relationships in Japanese macaques(Macaca fuscata)

Abstract This study investigates the development of mother‐infant relationships in captive Japanese macaques (Macaca fuscata) in order to test the hypothesis that age‐related changes in monkey mother‐infant interactions are primarily mother‐driven. During the first week of their life, infants spent about 90% of the observation time in ventroven‐tral contact with their mother. As the infants grew, time in ven‐troventral contact decreased progressively. This decrease was associated with an increase in the tendency of the mothers to reject the infants’ attempts to gain ventroventral contact and to an increase in the infants’ role in maintaining such contact. A decrease in the tendency of the mothers to protect the infants and in the proportion of attuned locomotion due to maternal carrying was also observed. A relatively high degree of developmental consistency was shown to exist in the interdyadic differences observed, but these differences could not be unambiguously ascribed either to differences among mot...