Reproduction and social rank in female stumptail Macaques (Macaca arctoides)

Reproductive physiology was studied in female stumptail macaques. Initially the monkeys were housed indoors (individually and in small groups) and later as one large (92 individuals) social group in an outdoor cage. Most data were collected during the 4-year outdoor period. Plasma progesterone determination in blood samples taken at weekly intervals allowed estimation of ovulation and conception dates. The age at first ovulation (X =3.73 years) was positively correlated with body weight at 3 years of age. The average age at first birth was 4.90 years. Gestation lengths averaged 176.6 days. Following a live birth ovulations returned after a mean interval of 11 months but following an abortion or still birth this interval was 1 month. Usually a number of ovulatory cycles (X =2.37) preceded a conception. Interbirth intervals (IBIs) in the outdoor cage (X =619.4 days) were significantly longer than IBIs during the indoor period (X =523.1), because indoors the infants were weaned at the age of 7 months, while outdoors weaning occurred more naturally. IBIs following abortions or still births (X =291.9 days) were significantly shorter than IBIs following live births. Age at first ovulation, age at first birth, IBIs, and infant production rates were not correlated with dominance rank. Ovarian cycle lengths (X =30.2 days, mode = 28 days) were comparable to previously reported data from laboratory-housed stumptails. No systematic seasonal fluctuations were found in the onset of sexual maturity, in ovarian cycle lengths, in copulation frequencies, and in distribution of births.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Group Fission in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed eight group fissions occurring during a 20-year period in three groups of a free-ranging provisioned Barbary macaque population. The founder group fissioned four times within 3.5 years after transfer to the enclosure, indicating that external factors—new environment, more space, absence of other groups—facilitated group fissions. Two groups resulting from these fissions, split twice within 2.5 and 1 years, respectively, many years later. The process of fissioning lasted from a few months to almost 2 years. Fissions were preceded by peripheralization/subgrouping of mainly young adult males (8-10 years old), suggesting that male competition was the primary force for the fissions. The males were joined by middle- to low-ranking but not the lowest-ranking females. The resulting new groups were usually smaller than the groups in which the former -matriline—old groups—stayed, and they were also more variable in size and sex ratio, suggesting that variable numbers of surplus individuals were expelled during fission. Mean adult sex ratios were similar in both groups after fission, indicating that the competitively superior males in the old groups (groups + -matriline) could not increase their breeding opportunities. Female kin, even of large matrilinies, almost always stayed together during fission. Natal males strongly preferred to join the old groups, and this preference was most pronounced in juveniles and subadults. Hence, most natal males stayed with maternally related females, i.e., remained true natal males, if the females stayed in old groups. They were separated from female kin, i.e., became seminatal, if the females joined the new groups. These seminatal males did not differ from natal males with respect to matrilineal rank, but they had more female relatives, above all more close relatives (sisters), indicating that avoidance of mating with maternal kin was important for group choice. Despite joining the same group as female kin during fissioning, breeding opportunities of natal males (ratio of unrelated females/male) were not less than that of their seminatal peers, because natal males had fewer female relatives. Only a minority of both groups of males would have done better by joining the alternative group. Paternal relatives were distributed during fission by chance, and loss of patrilinies was therefore much less pronounced. We conclude that the rules governing social relationships among Barbary macaque males are less apt to cope with the high number of males resulting from provisioning, whereas the rules regulating social relationships of females living in a nepotistic, female-bonded society are very robust in this respect.     

Perception of stimuli presented as photographic slides in cynomolgus macaques (Macaca fascicularis)

The present study was designed to assess a monkey's perception of specific visual stimuli by measuring both the behavioral responses and duration of attention to the presentation of photographic slides. Five adult male cynomolgus macaques (Macaca fascicularis) were placed individually in an open field apparatus and presented a series of slides consisting of apples, a gorilla mask, a collage of colors, a human being, and a plain field. The slide of the gorilla mask followed by that of the human being received the most attention while the plain field received the least. In addition, the gorilla mask and human being elicited a range of behavioral responses with the higher ranking animals displaying a greater number of aggressive responses and the lower ranking animals displaying a greater number of submissive gestures. Taken together, these data would suggest that the slides of the gorilla mask and the human being were perceived by the monkeys as threatening. These results are consistent with a continuing theme observed among a number of studies of primate social perception — namely, that potentially threatening stimuli are a significant determinant of visual observing.     

Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis)

Summary The seeds in fruits consumed by primates may be chewed and digested, swallowed and defecated intact, or separated from the flesh and spat out. We show by a combination of close field observations and experiments with caged animals, that long-tailed macaques (Macaca fascicularis) have a remarkably low threshold of 3–4 mm for swallowing seeds and also that wild macaques rarely break them. The seeds of 69% of the ripe fruit species eaten are spat out intact or cleaned outside the mouth and dropped. Seed-spitting significantly reduces the swallowed food bulk and may lessen the risk of releasing seed toxins during mastication. However, it requires that even small fruits are processed in the mouth one or a few at a time. We suggest that fruit storage in the cheek pouches of cercopithecine monkeys allows them to spit seeds individually without excessively slowing fruit intake while feeding on patchily distributed fruit. In contrast, Apes and New World monkeys apparently swallow and defecate most ripe seeds in their diet and colobine monkeys break and digest them, detoxifying seed defenses by bacterial fermentation.     

Development of the brain in staged embryos of the long-tailed monkey (Macaca fascicularis)

The external characteristics and successive morphological changes of the brain and its derivatives were studied in 69 long-tailed monkey embryos representing developmental stages 8 through 16. This morphogenesis follows a similar pattern to those of the rhesus, baboon, and human. Minor differences in the temporal sequence of specific developmental events include: 1) otic disc, adenohypophyseal pouch, and hippocampal internal sulcus formation in the long-tailed macaque occur at stage 10, stage 11, and after stage 16 respectively, which is comparable to human stages 9, 10, and 16; 2) formation of the trigeminal primordium and the motor root of the trigeminal nerve and evagination of the neurohypophysis occur at stage 12, stage 14, and stage 15, while in the human embryo these features are observed at stage 14, stage 15, and stage 16, respectively; and 3) closure of the lens pore, like in the rhesus monkey, occurs during stage 15, while in the baboon and human it takes place during stage 14. These temporal differences in the embryonic period are important factors to be taken into consideration in any embryological and teratological studies when usingM. fascicularis as a primate model.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.     

Female menstrual cyclicity and sexual behavior in stumptail Macaques (Macaca arctoides)

The sexual behavior and female reproductive cycles of a captive group of stumptail macaques (Macaca arctoides)were monitored during a 12-month period. The data, consisting of 303 ad libitummounts and copulations and 125 hr of focal-female testing, were analyzed by their frequency of occurrence during the three hormonal phases of the female menstrual cycle. Regularly cycling females exhibited statistically higher frequencies of all sexual behaviors compared to the amenorrheal controls. Contrary to previous reports which indicate no variation in sexual behavior throughout the reproductive cycle in this species, our data show marked increases in copulations during the periovulatory phase. Male dominance rank is associated with sexual behavior only at midcycle.     

Feeding ecology of the long-tailed macaque(Macaca fascicularis) in Kalimantan Tengah,Indonesia

I studied long- tailed macaque (Macaca fascicularis)feeding behavior and ecology as part of a larger behavioral ecological study at the Natai Lengkuas Station, Tanjung Puting National Park, Kalimantan Tengah, Indonesia. I collected data on feeding behavior via scan sampling of all visible individuals in the focal group (approximately 800 observation hours). I established vegetational plots and monitored them monthly to determine food availability and abundance. I found long- tailed macaques to be primarily frugivorous;leaves, flowers, insects and bark provided the remainder of the diet. They used at least 33 plant species as food sources, but >60% of the diet was provided by only 5 species. Based on previous vegetational analyses, these tree species were among the highest in relative density. However, selection ratios for 19 food species indicate that 13 of them were selected more often than expected. Long- tailed macaques appear to be selective feeders but can exploit a variety of food sources during periods of food scarcity.     

Mobility of surrogate mothers and persistent neophobia in cynomolgus monkeys (Macaca fascicularis)

In search of the relevant difference between mother rearing and surrogate rearing with respect to the emergence of neophobic behavior in macaques, we tested the hypothesis that mobility of surrogate mothers prevents the development of neophobic behavior in cynomolgus macaques. The experimental group consisted of ten surrogate-reared subjects which during their first year got rides on surrogate mothers moving through the cage. The control group consisted of nine subjects reared with immobile surrogate mothers. Between the age of 7 and 27 months the reactions to two different novel objects were tested. First exposure to one object occurred at 6 months of age and to the other object at 20 months. The kind of object and the age of first exposure made no difference. Contrary to our expectations mobility of surrogates did not affect the incidence of neophobia: most subjects in both groups persistently avoided the objects. This finding seems to support Hofer's hypothesis that the mother acts as a regulator of the infant's behavior and physiology.     

Isolation and culture of hepatocytes from the cynomolgus monkey (Macaca fascicularis)

Summary Isolation and culture techniques for hepatocytes from whole livers of the cynomolgus monkey,Macaca fascicularis, are described. Hepatocytes were isolated by two-step perfusion of livers, using collagenase with hyaluronidase; fructose and trypsin inhibitor were included to reduce cell loss. Yields from a single liver average 4×10⁹ cells with viabilities of 90.8±5.7%. Cells, plated on collagen substrates, were assessed for changes in morphology and various marker enzyme activities over a period of 7 d in culture. Cells exhibited a morphology similar to that observed for this species in vivo; little change in attached and spread cells was observed over the length of time monitored. Enzyme activities for catalase, succinate dehydrogenase, and tyrosine aminotransferase were observed to decrease significantly (though considerable activity remained), whereas acid phosphatase and 5′-nucleotide phosphodiesterase remained unchange. Activity of cytochrome P-450 reductase was observed to increase slightly for the first 2 d, then decrease to about 60% of initial levels. Activity of α-mannosidase was stable for 4 d but was observed to be increased at Day 7. Cells were observed to retain metabolic responsiveness demonstrated by glucose production by both gluconeogenesis and glycogenolysis in response to glucagon stimulation. The monkey hepatocytes obtained by methods described here thus retain hepatocellular morphology and activity through at least 1 wk in culture without medium or culture modification.     

Genetic characterization of long-tailed macaques (Macaca fascicularis) on Tabuan Island Indonesia

Protein and mitochondrial DNA variations (D-loop region PCR-RFLP) were analyzed for 7 serum and 40 clot samples collected from long-tailed macaques (Macaca fascicularis) living on Tabuan Island, Indonesia. Protein polymorphisms were examined electrophoretically for 5 and 12 kinds of protein in serum and erythrocytes, respectively. Each of the protein loci tested showed a monomorphic pattern. Polymorphisms were detected in the analysis of the D-loop-containing region of mtDNA (PCR-RFLP) using 32 restriction endonucleases. Two haplotypes, differing 1.03% in sequence divergence were observed, and both were previously undetected in other local populations. Based on genetic features and differences in pelage color as outlined inFooden's (1995) morphological analysis, the present results suggest that long-tailed macaques on Tabuan Island are a unique population. From the genetic analyses performed here, Tabuan monkeys are considered to be the same species group as those populations of Sumatra and Java (Fooden, 1995).     

Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella)

The responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella) were investigated. In both species the amount of fear behavior was higher in the presence of the model than during baseline conditions. Unlike the macaques, in the capuchins the frequency of these behaviors decreased across trials. In the two species the amount of explorative and manipulative behaviors and the use of space were also different. Unlike macaques, all capuchins manipulated the objects available in the testing room, and three subjects contacted the apparatus by using objects. Macaques did not show significant preferences for any particular part of the testing room. In both conditions, capuchins used the floor more than macaques did. Further, capuchins increased the use of the floor across experimental trials. Latency to reach the floor was higher in macaques than in capuchins. When on the floor, capuchins spent most of the time close to the snake apparatus. It is proposed that the behavioral differences between capuchins and macaques in the responses to a potential predator indicate that capuchins have a greater propensity to explore and to contact the novel stimulus directly, or by means of objects, than macaques do. These tendencies may lead to the exploitation of novel features in the environment.     

Responses to urinary stimuli in pigtailed (Macaca nemestrina) and stumptailed (Macaca arctoides) macaques

Responses to different urine samples were studied in pigtailed (M. nemestrina) and stumptailed (M. arctoides) macaques. Both species exhibited more interest towards urine samples from their own species than neutral stimuli. Responses towards urine samples from other macaque species did not significantly differ from those towards neutral stimuli. In stumptailed macaques, no differential interest was observed between urine samples from a known (the adult male of the group) and an unknown adult male conspecific.     

Gestation length in rhesus macaques (Macaca mulatta)

We describe some of the sources of variation in gestation length among rhesus macaques. the data were obtained from the timed-mating breeding program at the California Regional Primate Research Center (CRPRC). Information about approximately 700 pregnancies that resulted in spontaneous vaginal deliveries of liveborn young is presented. The average length of these pregnancies was 166.5 days. In this population, older females with higher parities had significantly longer pregnancies and significantly heavier infants than other females did. Other factors, including infant sex, month of conception, maternal reproductive history, and paternal identity, had no consistent effect upon gestation length.     

Group Fission in Moor Macaques (Macaca maurus)

This is the first report of group fission in a wild group of Moor macaques (Macaca maurus) in South Sulawesi, Indonesia. The subject group, which has been observed on the basis of individual identification since 1988, showed no sign of fission in April 1999. In August 1999, the group had split in two, with the same number of mature females in each new group. For the most part, mothers and their offspring joined the same groups. Dominance relations and association patterns established during the previous year among adult females did not strongly affect new group membership. The difference in female reproductive state between the two branch groups was a prominent characteristic. The -male of the original group visited both groups at the first stage of group fission, even though otherwise the compositions of the new groups were stable. After the division, six adult males from outside the original group immigrated exclusively into the group that did not contain the -male of the original group. Severe intergroup encounters occurred between the two groups. We discuss the process of the fission and the resultant pattern in relation to the egalitarian dominance style among females, lack of seasonality in reproduction, and resemblance to one-male type social organization.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.