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.     

Environmental temperature and reproductive seasonality in Japanese macaques (Macaca fuscata)

This study demonstrates that the reproductive seasonality ofMacaca fuscata seems to be more affected by environmental temperature than by photoperiod. Mean conception dates for 25 groups of Japanese macaques species did not correlate with latitude. Instead, they were positively related to mean fall and winter temperatures and negatively related to the magnitude of the decrease in the mean temperature from summer to fall. Evidence from transplanted groups supports the hypothesis that environmental temperature is a decisive factor in determining the timing of mating activities of Japanese macaques. These results are also consistent with the concept that, in temperate zones, environmental temperature is probably the best indicator of local climatic characteristics.     

Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

Ecology of rhesus macaques (Macaca mulatta) in northwest Pakistan

The feeding ecology of rhesus monkeys,Macaca mulatta, was studied between 1978 and 1981. The study site, located in the Murree Hills of northwestern Pakistan, supported a mixed coniferous-deciduous forest community and was characterized by a high degree of human disturbance. We used a linear transect method to sample the species composition and structure of the vegetation. Comparison of these data with historical records showed that the forest has undergone major changes in the last hundred years. Data on feeding behavior were collected through on-the-minute focal animal sampling. The monkeys spent about 45% of the day feeding. Their preferred foods were grass, clover, and other ground herbs that occur in the disturbed sites. Fruit accounted for less than 9% of feeding records. The rhesus monkey may be pre-adapted to living in disturbed-site, forest-edge communities. The evolutionary history of Macaca mulatta may be tied closely to the disappearance of forest and the spread of meadows and savannahs over the last million years.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

Live birthrates in two free-ranging rhesus breeding colonies in the Florida keys

The present paper provides an analysis of reproductive data derived from 1,265 adult female rhesus monkeys (Macaca mulatta), including 570 animals 13 years old and older. The data were collected during a partial census of two provisioned but free-ranging rhesus populations in the Florida Keys. Within both colonies, live birthrates were found to increase sharply among females 4–7 years old and to decline linearly among females 7–17 years of age. These data do not support the suggestion byAnderson (1986) that decline in fertility among nonhuman primate females is primarily the result of deteriorating health rather than ageper se.     

Geophagy amongst rhesus macaques on Cayo Santiago,Puerto Rico

Soil mining and eating (geophagy) behavior of rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico, is described and assessed with respect to the chemical, geochemical, and mineralogical composition of the ingested materials. The samples forming the uneaten (control) and eaten (matrix and blocky) groups of soils come from the top and flanks of a marine terrace underlain with volcanic tuff on Cayo Santiago, off the east shore of Puerto Rico. Both the uneaten and geophagy samples were analyzed to determine particle size distributions, clay and primary mineralogy, and soil chemical and geochemical compositions. Primary minerals such as orthoclase and plagioclase feldspar in the clay fraction is higher in the control group than in the ingested samples. Both the control and matrix plus blocky samples have moderate to abundant amounts of kaolinite and halloysite (both silicon:aluminum = 1:1 type clay minerals) that may be important as a stimulus to geophagy behavior. The pH, total salts, and phosphorus levels in both the control and geophagy samples show considerable overlap with little clear indication of causal factors. Analysis of the geochemical data showed no clear cut elemental differences to suggest elemental supplementation as a possible explanation for mining and eating of tropical soil. It is possible that rhesus macaques ingest clay to obtain kaolinite/halloysite minerals which may alter the taste of their provided food, and may act as pharmaceutical agents to alleviate intestinal ailments such as diarrhea.     

Copulatory behavior in a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico

This paper presents copulatory data gathered on a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico. The study found evidence for seasonal clumping of matings, with the peak in the month of February, and that matings are more common in the afternoon, when measuring diurnal changes. It also found that males require an average of one and a half mounts before ejaculating, and mating among females is distributed unequally, when the measurement is between those females that mated. Furthermore, male dominance rank and male-female affiliation are both positively correlated with mating frequency. Variations between this study and captive studies are minimal. The variances that do occur may be explained by differences in the research settings or the individual differences in the subjects' behavior across studies.     

4040 SNPs for genomic analysis in the rhesus macaque (Macaca mulatta)

Although the rhesus macaque (Macaca mulatta) is commonly used for biomedical research and becoming a preferred model for translational medicine, quantification of genome-wide variation has been slow to follow the publication of the genome in 2007. Here we report the properties of 4040 single nucleotide polymorphisms discovered and validated in Chinese and Indian rhesus macaques from captive breeding colonies in the United States. Frequency-matched measures of linkage disequilibrium were much greater in the Indian sample. Although the majority of polymorphisms were shared between the two populations, rare alleles were over twice as common in the Chinese sample. Indian rhesus had higher rates of heterozygosity, as well as previously undetected substructure, potentially due to admixture from Burma in wild populations and demographic events post-captivity.     

Aggressive intergroup encounters in two populations of Japanese macaques (Macaca fuscata)

It is predicted that variation in intergroup relationships in group living primates reflects the cost and benefit of resource defense. We tested the applicability of the model by examining population difference, group difference, and seasonal difference in behaviors during intergroup encounters in two populations of Japanese macaques (Macaca fuscata), one of six groups from Yakushima Island, and the other of three groups from Kinkazan Island. We found that the nature of intergroup encounter varied with group identity, reproductive seasonality, and population. Yakushima groups showed aggressive behaviors more frequently than did Kinkazan groups and the difference was consistent with the food competition model, both because of the involvement of females, and because home ranges were smaller on Yakushima than on Kinkazan, and thus more defensive. Both sexes of animals participated in aggressive interactions, but males were more aggressive than females. Furthermore, Yakushima population showed more agonistic intergroup behaviors during the mating season than the non-mating season. Also during the encounters, intergroup mating was observed, but only in Yakushima. It is concluded that intergroup relationships reflect the mate guarding behavior by group males. However, the agonistic relationship during non-mating season, especially that of among females, is also consistent with the food competition model. It is also noted that males' behavior toward other groups can also be interpreted as a form of investigative behavior before possible transfer into a new group.     

A 15-year study of the association between dominance rank and reproductive success of male rhesus macaques

The reproductive success (RS) of 32 males in a captive group of rhesus macaques (Macaca mulatta) between 1978 and 1992 was determined using paternity exclusion analysis. Dominance rank of each male over age 4 was assessed at the end of each breeding season based on agonistic dyadic interactions. The dominance rank and RS of these males were strongly correlated whether or not subadult males were included. The high reproductive success of males that eventually reached alpha rank is primarily responsible for this outcome. These results support the theory that social dominance has evolved in genusMacaca by sexual selection but some changes in male dominance rank and RS during the 15-year period suggest that priority of access is not the sole focus for such selection.     

Breeding seasonality among long-tailed macaques,Macaca fascicularis,in Peninsular Malaysia

The females among more than 7000 long-tailed macaques, Macaca fascicularis,that had recently been trapped for biomedical research were examined for pregnancy. The animals were taken from the wild in the north of Peninsular Malaysia during the period 1978 to 1979 and in the south from 1978 to 1982. Both samples showed some pregnancies in all months of the year and a peak during the months of May to July. Additional peaks in other months in some years showed that, while the midyear pregnancy peak was significant, it was not as marked a phenomenon as is the breeding peak in many other species. This might be due to the complexity and unpredictability of both the climate and the macaques’ food supply in Peninsular Malaysia. The additional peaks also illustrated the pitfalls of generalizing about breeding seasonality on the basis of small samples.     

Varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta)

The behaviour of members of a group of rhesus monkeys was observed in experimentally created, competitive feeding situations. Socially dominant members of the group tended to start eating before lower-ranking subjects, and generally ate more. Dominants sometimes used aggression to control access to food, but overall, intermediate-ranking monkeys were involved in most agonistic episodes. Non-dominant subjects improved their feeding performance when food was presented in three piles rather than one pile, often by snatching food and consuming it away from the pile. These general patterns were less evident when realistic snake models were placed on some of the food piles. Feeding was disrupted by the presence of snakes, but notably, subordinates risked feeding in these conditions. Piles containing preferred foods and snakes were eaten from, but a low-preference food (carrot) under snakes went untouched by all subjects. The results suggest that group-members evaluate potential risks and benefits of competing for a restricted resource, and that dominance status, while an important factor, is only one element in the equation.     

Birth seasonality and interbirth intervals in free-ranging formosan macaques,Macaca cyclopis, at Mt. Longevity, Taiwan

Thebirth season of Formosan macaqueM. cyclopis during our study started in February and ended in August with a peak in the second half of April and the first half of May. The average birth rate was 82%±21 for 114 females with four years of breeding records. Our study reports that a time span of one year between births can be considered as the norm for the wildM. cyclopis. Of the 288 inter-birth intervals (IBI), 88.5% showed a 1-year interval (mean 364±SD 29 days); 11% showed 2-year interval (727±36 days); and 1% (2 females) had 3-year interval (range 1030–1040 days). The IBI for females that had infant loss within six months of life were the shortest. But there was no significant difference from that of females that had stillbirth (p>0.9) and infant that survived for first six months of life (p>0.06). However, among 255 cases of 1-year IBI, stillbirth or following infant loss within six months of life did significantly shorten IBI for ten days (F _1,253=5.74,p<0.05).     

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.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Aspects of fight interference in free-ranging and compound-dwelling rhesus macaques (Macaca mulatta)

Patterns of fight interference (agonistic aiding) were compared among three groups of rhesus monkeys (Macaca mulatta) living in two settings: (1) two groups at Cayo Santiago (Caribbean Primate Center); and (2) one group at the Yerkes Regional Primate Research Center (YRPRC). A total of 1,227 interference episodes were recorded in 1,650 hours of observation. The only significant intergroup difference was the increased tendency of males at YRPRC to aid aggressors rather than victims. Among other findings, females aided relatives, interfered against target animals dominant to themselves, aided juveniles, and aided victims more consistently and frequently than did males. Importantly, female interference became more male-like in pattern when aid was given to nonrelatives. Neither the dominant males nor males in general displayed a unique or consistent tendency to interfere in fights in a manner which could be interpreted as controlling aggression. The males' interference patterns also did not suggest they were forming coalitions to either attain or defend status rankings. It is concluded that, overall, observations of compound-dwelling and free-ranging rhesus monkeys reveal similar relationships. Further, while female rhesus monkeys interfered in fights in a manner consistent with the control of aggression and protection of kin, the motives of male interferers remain unknown; however, their behavior is consistent with the hypothesis that they were reducing intermale tensions while, at the same time, minimizing physical risk.     

Biochemical genetics of macaques. I. 6-phosphogluconate dehydrogenase polymorphisms in Macaca mulatta and Macaca speciosa

Starch gel electrophoresis of erythrocytes from 1812 Macaca mulatta has unequivocally demonstrated that the 6-phosphogluconate dehydrogenase (6PGD) isozymes are controlled by two autosomal codominant alleles. Limited data on erythrocytes from 89 Macaca speciosa were also consistent with autosomal codominance.This work was supported in part by NIH Grants HD 07835 (WHS) and RR-00167 (Wisconsin Regional Primate Research Center) and by the Research Committee of the UW Graduate School (Project No. 170207).Paper No. 2146 of the Laboratory of Genetics, and Publication No. 16-045 of The Wisconsin Regional Primate Research Center.