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.     

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.     

Return-benefit spite hypothesis: An explanation for sexual interference in stumptail macaques (Macaca arctoides)

Sexual interference behavior (the phenomenon of intervening with the matings of others) appears selfish in that its primary function seems to be that of improving one's reproductive fitness relative to others. In stumptail macaques (Macaca arctoides), interference may be spiteful, and may contribute to the receipt of a return benefit. This is the focus of this paper. The subjects were 58 stumptail macaques in a single group with seven matrilines. They were free-ranging, habituated to human observation, and lived on the island of Tanaxpillo at Lake Catemaco in southeastern Mexico. During the study, tie durations (the periods where male and female genitalia remain connected following ejaculation) were significantly altered overall, being longer, on average, during matings with sexual interference, opposed to those without interference. When matings occurring in succession were divided in half, ties were significantly longer during the second half than the first half. Also, although the difference was not statistically significant, the average number of mounts required by males to reach ejaculation was greater during matings with interference than without interference. Such apparent social stress may reduce the fertility of the mating pair at some cost to the interferer. Some individuals that interfered also used alternative mating tactics. These matings were 27% of the total, and they received interference less often than normal matings. When alternative matings were interfered with, they received significantly less interference: alternative matings received nearly eight times less interference than normal matings. The average tie duration for alternative matings without interference was also significantly less than the average tie for normal matings with interference. Alternative mating tactics appear to elicit less social stress; this may contribute to increased reproductive fitness for individuals that practice both alternative mating and sexual interference, if the latter produces a return benefit.     

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.     

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.     

Heterosexual interactions of pairs of laboratory-housed stumptail macaques (Macaca arctoides) under continuous observation with closed-circuit video recording

Female-male interaction of heterosexual pairs of stumptail macaques, housed together continuously, was studied 24 hr per day using closed-circuit video recording. Two pairs were studied for approximately 2 months each. Although no generalizations can be made from such a small sample, no aspect of behavioral interaction varied significantly with the stage of the menstrual cycle of the female partner. Copulation occurred regularly but only during the daylight hours. Both pairs showed several peak ejaculation days (5–21 ejaculations/day), which were distributed throughout the entire menstrual cycle. In general, the highest number of ejaculations was observed to occur when the animals were put together either for the first time or following a separation of a few days. In one pair the female became pregnant, and from the fifth week of pregnancy onward there was a gradual increase in male aggression, coinciding with a decrease in male sexual and grooming behavior. In a second study eight different pairs were observed during the first day together and male copulatory behavior was studied. Two patterns of copulatory behavior could be discerned: pairs displaying a high number of ejaculations (19–38) and pairs displaying a low number of ejaculations (4–8). With regard to the interejaculatory interval (IEI), the male stumptail appeared to be unique. In contrast to what has been reported for other mammals, i.e., a steady increase in IEI with subsequent ejaculations, the stumptail showed increasing IEIs only during the first three to four, as well as between the last, ejaculations; in between, the IEI remained relatively constant. The maximum number of consecutive ejaculations observed was 38, displayed during a 10-hr time period (mean (± SEM)IEI, 12.9 ± 3.5 min).     

Responses to animal stimulus photographs in stumptailed macaques (Macaca arctoides)

Interest in their animate environment was studied in a captive group of 11 stumptailed macaques (Macaca arctoides). Subjects were shown projected photographic slides, most of which showed a single individual primate or non-primate. The measure of interest was the duration of viewing. Results showed that adult females exhibited more interest towards stumptailed macaques versus other macaques species, and towards adult females carrying infants versus adult females alone. Data concerning non-primates showed that subjects were especially interested by photographs of felids; this effect was partly due to the presence of two frontal and conspicuous eyes in felids.     

Social communication among captive stump-tailed macaques (Macaca arctoides)

I compared the frequency of occurrence, contextual usage, and meaning of some of the most prominent gestural signals in stump-tailed macaques. I recorded the occurrence of 15 visual and tactile behavior patterns in a multimale multifemale captive group of stump-tailed macaques with the behavior sampling method in 100 hr of observation and analyzed the data via factor analysis and analyis of variance. The hindquarter presentation was the most frequent gesture. It was displayed by subordinates to appease dominants even in the absence of impending risk of aggression. Bared-teeth, lip-smack, teeth-chatter, and present-arm are submissive signals as well, but they differ from the presentation and from one another in their contextual usage. Nonthrusting mount, hip-touch, hip-clasp, and genital manipulation are directed down the hierarchy and appear to reflect dominance, reassurance, protection, or bonding. Mock-bite is a ritualized aggressive behavior pattern, often used to resolve uncertain dominance relationships. Ventroventral embrace occurs as a female bonding pattern. Overall, most gestural signals in stump-tailed macaques relate to dominance and submission and, to a lesser extent, social bonding.     

Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

Patterns of sexual behavior in male macaques

One large social group of each of three species of macaques (Macaca mulatta, M. fascicularis, M. radiata), housed in half-acre field cages at the California Primate Research Center, were observed for a total of 150 h. Data on sexual behavior and dominance interactions were recorded by pairs of experienced observers using a focal animal technique. Single or multiple mount-to-ejaculation sequences, number of thrusts per mount, number of mounts per sequence, duration of mounts per sequence, duration of sequences, social rank and frequency of sexual activity were recorded for each adult male. M. mulatta used a multiple mount-to-ejaculation (MME) pattern in 91% of their copulations. M. radiata used a single mount-to-ejaculation (SME) pattern in 91% of their copulations. M. fascicularis used both patterns—53% MME and 47% SME. A positive correlation was found between rank and sexual activity in fascicularis and mulatta males. A negative correlation between rank and sexual activity was found in radiata males and also a positive correlation between rank and age indicating that the youngest and most subordinate radiata males were the most sexually active males. In reviewing the literature, a relationship between degree of intermale competition, intermale tolerance and type of mounting pattern was revealed. Macaque species that primarily use an SME pattern also show sa high degree of intermale tolerance and little interrnale competition. Macaque species that primarily use an MME pattern typically show a high degree of intermale competition and a low degree of intermale tolerance. Possible events leading to such relationships are discussed.     

A statistical analysis of the social behavior of the male stumptail macaque (Macaca arctoides)

The social behavior of male stumptail macaques was analyzed in terms of behavioral sequences recorded during paired encounters in a large test cage. Recurrent patterns of behavioral sequences were sought and used to hypothesize the structure of motivational systems of social behavior as has been done previously for other species. In addition to traditional statistical analyses to determine which dyadic behavioral sequences were nonrandom, there were several methodological innovations. Instead of analyzing behavior as a single channel of communications, we analyzed three independent channels and considered their inter-correlations: 1) acts and postures; 2) vocalizations; and 3) facial expressions. Also, we analyzed not only within-animal behavioral sequences but between-animal sequences as well. Results were derived from 40 tests, most of which included vigorous agonistic and sexual interactions and a behavioral repertoire similar to that of adult male stumptail macaques observed by previous investigators. There were 30 acts and postures, eight facial expressions, and seven vocalizations that occurred more than five times. Many acts and postures occurred in nonrandom sequences, 43 such sequences within-animal and 40 between-animal. From these sequences and their correlations with specific vocalizations and facial expressions, it was possible to differentiate six categories of social behavior that may correspond to six different motivational systems: offense, defense, submission, groom and contact, male sexual behavior, and display. Both the frequency of behaviors in each category and the nature of the behavioral sequences were affected by the relative dominance of the two animals.     

Close bonds and social rank similarities favor non-random mating in captive stump-tailed macaques (Macaca arctoides)

Assortative mating is non-random mating by the mutual choice of phenotypes or behavioral types. In polygynandrous species, competition for mating by social rank can lead to assortative mating. However, although not an individual trait, social bonds also influence mating opportunities resembling assortative mating. Stump-tailed macaques form long-term close bonds and organize in a linear dominance–subordination hierarchy. Therefore, we studied whether the strength of the social bond and rank closeness influenced mating decisions and increased mating opportunities, particularly for low- and middle-ranking animals. Firstly, we observed whether females directed proceptive behavior to close-bonded or adjacent rank males. Secondly, we measured whether successful copulations were related to the strength of social bonds and close ranking. Thirdly, to ensure that copulations owed mainly to the aforementioned factors, we also evaluated whether sexual coercion was unrelated to social bonds and rank similarities. Finally, we assessed whether close bonds mediated agonistic support to females. The study subjects were 12 adult female and 11 male captive stump-tailed macaques. We monitored daily females' reproductive status by vaginal cytology. Sexual behavior was recorded by all occurrences sampling and scan sampling to collect the agonistic and affiliative instances required to calculate social ranks, social bond strength, and agonistic support. The results indicated that the probability of females displaying proceptivity increased during the follicular phase toward close-bonded and high-ranking males. Copulation chances increased with male–female social bonds and rank closeness. Forced copulation decreased in close-bonded individuals, while agonistic support increased in close-ranking strong-bonded animals. In conclusion, close social bonds and similar social rank result in non-random mating in stump-tailed macaques.     

Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although female catarrhine primates show cyclic changes in sexual behavior and sexual swellings, the value of these sexual signals in providing information to males about timing of the fertile phase is largely unclear. Recently, we have shown that in Barbary macaques, males receive information from females which enables them to discern the fertile phase and to focus their reproductive effort accordingly. Here, we investigate the nature of the cues being used by examining female sexual behavior and the size of sexual swelling as potential indicators of the fertile phase. We collected behavioral data and quantified swelling size using digital images of 11 females of the Gibraltar Barbary macaque population and related the data to the time of ovulation and the fertile phase as determined from fecal hormone analysis. We found that rates of female sexual behaviors were not correlated with female estrogen levels and did not significantly differ between the fertile and non-fertile phases of the cycle. In contrast, swelling size was significantly correlated with female estrogen levels and increased predictably towards ovulation with size being maximal during the fertile phase. Moreover, frequencies of male ejaculatory copulations showed a strong positive correlation with swelling size and highest rates were found during maximum swelling. Our data provide strong evidence that female Barbary macaques honestly signal the probability of fertility through sexual swelling and that males apparently use this information to time their mating activities. Honest advertising of the fertile phase might be part of a female strategy to manipulate male mating behavior for their own advantage, such as ensure fertilization with high quality sperm or influence paternity outcome.     

Video-induced yawning in stumptail macaques (Macaca arctoides)

This study reports the first experimental exploration of possible contagious yawning in monkeys. Twenty-two stumptail macaques (Macaca arctoides) were presented with video clips of either yawns or control mouth movements by conspecifics. At a group level, monkeys yawned significantly more often during and just after the yawn tape than the control tape. Supplementary analysis revealed that the yawn tape also elicited significantly more self-directed scratching responses than the control tape, which suggests that yawning might have been caused by tension arising from viewing the yawn tape. Understanding to what extent the observed effect resembles contagious yawning as found in humans and chimpanzees requires more detailed experimentation.     

A comparison of the behavior of Macaca fascicularis and Macaca mulatta in relation to the menstrual cycle

Observations on oppositely sexed pairs of M. fascicularis and M. mulatta revealed certain differences. M. fascicularis showed single-mount copulations, higher potency, less grooming activity, and milder but more frequent aggressive exchanges than the rhesus monkey. These differences might be due to the lower dominance gradient between the sexes and less sexual dimorphism in M. fascicularis than in M. mulatta. There were changes in the sexual, grooming, and aggressive interaction in relation to the menstrual cycle, indicating the suitability of M. fascicularis for hormone-behavior studies. Comparison of data from 30 and 60 min tests showed that important behavioral changes did not become apparent unless animals were given enough time to interact.     

Sexual strategies of female Japanese macaques (Macaca fuscata)

Evidence is reviewed that female Japanese macaques have multiple male mating partners when they are available and show a preference for mating with sexually unfamiliar males. Several lines of evidence suggest that this aspect of female sexual behavior results in the offspring of an individual female being sired by more than one male thereby maintaining the genetic diversity of the troop. Evidence is presented in this paper that a decrease in the number of adult troop males and a lack of extra-troop migrant males in the Arashiyama West troop of Japanese macaques following transplantation to a ranch in south Texas had consequences for the sexual behavior of the females.     

Non-seasonal breeding pattterns in stumptail macaques (Macaca arctoides)

This paper summarizes published reports of breeding patterns across the genusMacaca. Patterns range from strictly seasonal to non-seasonal. Data on sexual behavior and birth patterns are presented which confirm previous reports of non-seasonality forMacaca arctoides. In a captive colony, 63 births were recorded, and individuals were born during every month of the year. Heterosexual mounting activity was recorded over a two-year period and occurred during every month of that period. It is clear thatM. arctoides does not exhibit the seasonal cyclicity observed in some other macaque species.     

Social and menstrual cycle phase influences on the behavior of group-housed Cebus apella

This study examined sexual and other social behavior in relation to menstrual cycle phase in four mixed-sex social groups of Cebus apella. Groups consisted of two adult males and either six or nine adult females. Menstrual cycles of high (rank 1–2) and low (rank 3–7) dominance-rank females from each group were monitored via vaginal swabs, and correlated with data collected from ongoing behavioral observations. Only cycles bounded by positive detection of menstrual blood were included in this analysis (n = 15 females, 182 cycles; mean ± s.d., cycle length = 20.8 ± 1.2 days). Rates of copulation and female solicitation of males varied significantly with cycle phase, with highest rates at midcycle. While total rates of solicitation and copulation did not vary with female dominance rank, copulation rates with the dominant male were significantly greater for high ranking females than for low ranking ones. Variance observed in affiliative and agonistic behaviors, including those with males, was attributable to female rank rather than cycle phase. Females and males were also observed attempting to interfere with copulations of lower ranking same-sex individuals. Although further study, particularly of wild populations, is needed, these results indicate that female-female reproductive competition should be included as a component of the capuchin breeding system. As in other primate species, both social and hormone-related factors influence the sexual behavior of Cebus apella. © 1995 Wiley-Liss, Inc.