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.     

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.     

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.     

Menstrual-cycle phase and sexual behavior in semi-free-ranging stumptail macaques (Macaca arctoides)

The sexual behavior and female reproductive cycles of a group of island-dwelling stumptail macaques (Macaca arctoides)were monitored over a 6-month period, yielding 530 observation hr and 268 copulations. Compared to nondominant males, the dominant male copulated at a relatively high rate throughout the cycle, but largely with one high-ranking female. The non-dominant males copulated most frequently at midcycle. Female presenting was highest at midcycle, but only to the dominant male. Cross-study discrepancies may be due to different observation methods and restricted environmental conditions that mask female-initiated sexual behavior. The more naturalistic setting of this study allowed for a fuller expression of proceptivity. Contrary to some previous conclusions, present findings suggest that both hormonal and socioenvironmental factors influence the patterns of sexual behavior found in stumptail macaque colonies.     

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.     

Development of co-feeding relationships in immature free-ranging Japanese monkeys (Macaca fuscata fuscata)

The co-feeding relationships of immature Japanese monkeys in the provisioned situation were studied. The most frequent co-feeders for immature females were diversified as compared to those for immature males. The number of immature females who showed strong co-feeding relationships with their mothers gradually decreased with age in both high- and middle/low-ranking matrilines, but the percent decrease was greater for middle/low-ranking immatures. Almost all immature females who displayed strong co-feeding relationships with adult males were from middle/low-ranking matrilines. Strong co-feeding relationships with mothers among immature males from high-ranking matrilines remained until 4 years of age. In contrast, strong co-feeding relationships with mothers among middle/low-ranking immature males decreased rapidly in the first year of life, and most 1- to 4-year-olds showed no strong co-feeding relationships with other group members. It is considered that middle/low-ranking mothers may not provide their immatures with a secure base for obtaining food in the provisioned situation.     

Localization of inhibin/activin subunits in the testis of adult nonhuman primates and men

The localization and distribution of inhibin/activin subunits was evaluated in the testes of three nonhuman primate species (Macaca fascicularis, M. mulatta, M. arctoides), of young (31 to 43 years) and old (60 to 85 years) men, and of men with disturbed or arrested spermatogenesis using immunohistochemical techniques (peroxidase-anti-peroxidase and alkaline-phosphatase/ anti-alkaline-phosphatase technique). Specific polyclonal (anti-porcine inhibin -1-32 and anti-bovine activin A) and monoclonal (anti-human inhibin -1-32 and anti-human activin A-82-114) antisera were employed. Among all nonhuman primate species and in men, inhibin/activin subunits were present in the cytoplasm of Sertoli cells and Leydig cells but not in germ cells. No relationship could be established between the staining pattern for inhibin/activin subunits and the completeness or the stage of the spermatogenic process. The staining for the A-subunit in Sertoli cells appeared more intense in the testes of old men compared with that of young men. The majority of Leydig cells contained either the -subunit and A-subunit or the A-subunit alone. The signal for the A-subunit was remarkably intense in normal and hyperplastic human Leydig cells. These observations demonstrate the presence of inhibin/activin subunits in Sertoli cells and Leydig cells of adult primates and raise the possibility that these subunits or their respective dimers (inhibin A/activin A) might subserve a paracrine/ autocrine role in the adult primate testis. Also, the possibility of specific differences in the -1-32 subunit and the A-82-114 subunit region among certain primate species arises from the observation that the monoclonal antisera failed to detect the respective antigens in M. fascicularis and M. mulatta.     

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).     

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.     

Rhesus macaque copulation calls: Re-evaluating the “honest signal” hypothesis

Male rhesus macaques sometimes give loud calls while thrusting or dismounting during multi-mount copulations.Hauser (1993) has proposed that these calls (1) impose a cost (increased risk of aggression) on calling males, and (2) increase callers' copulation frequencies, supporting the hypothesis that calls function as honest signals (handicaps) that females use to evaluate male quality during mate choice. This hypothesis was re-examined using data collected at Cayo Santiago, Puerto Rico on 40 focal females and their 56 observed copulatory partners. Although attacks by males against copulating pairs were frequent, they were usually directed only against the female of the pair. Males that called were no more likely than silent males to suffer male escalated attack during or immediately following mount series. Male-female dyads in which the male called during copulation were significantly more likely than non-calling dyads to complete the most copulations observed for any given female. Males that called at least once were significantly more likely than non-calling males to complete at least one copulation with a peri-ovulatory female. A log-linear model revealed that male rank and calling were both associated with likelihood of experiencing at least one peri-ovulatory copulation. However, calling was not associated with reception of demonstrated female mate choice behaviors. Controlling for dominance rank, callers did not experience more female proximity maintenance than non-callers. Nor were callers' hip-grasps refused less frequently than non-callers' hip-grasps. These results cast doubt on the hypothesis that rhesus macaque copulation calls are costly, honest indicators of intrinsic male quality. A contrasting alternative hypothesis, that a male's copulatory calls advertise relative immunity from attacks against his copulatory partners, was not supported either. Thus, the function of rhesus macaque copulatory calls remains unknown. The unusually high rate of copulations amongHauser's (1993) subjects may explain the discrepancy in results, but it is unclear how high copulation rates would increase the cost of copulatory calling to males.     

NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan

A macaque population produced by the hybridization of native Japanese macaques (Macaca fuscata) and introduced Taiwanese macaques (M. cyclopis) in Wakayama Prefecture was shown to possess three DNA haplotypes of the natural resistance-associated macrophage protein 1 (NRAMP1). Based on genotyping and comparison with M. fuscata populations, it was revealed that the introduced M. cyclopis population was polymorphic for the NRAMP1 locus. Extensive crossbreeding of the introduced species with the native species was confirmed using this genetic marker and the proportion of M. cyclopis genes was 57.4%. Results of statistical tests suggested non-random mating in the hybrid population.     

<Emphasis Type="Italic">Macaca munzala</Emphasis>: A New Species from Western Arunachal Pradesh,Northeastern India<Superscript>*</Superscript>

Macaca, comprising 20 well-characterized species, represents the largest and one of the most ecologically and socially diverse of all the nonhuman primate genera. We report the discovery of a macaque that is new to science from the high altitudes of western Arunachal Pradesh, a biodiversity-rich state in northeastern India. We propose the scientific name Macaca munzala and the vernacular name Arunachal macaque for the species. It shares morphological characteristics independently with the Assamese macaque (Macaca assamensis) and with the Tibetan macaque M. thibetana; like them, it appears to belong to the sinica species-group of the genus. However, the species is distinctive in relative tail length, which is intermediate between those of Tibetan and Western Assamese macaques, the subspecies with which it is sympatric. It is also unique in its altitudinal distribution, occurring largely at altitudes between 2000 and 3500 m. We provide a morphological characterization of the species, report preliminary data on its field biology and discuss possible taxonomic identity in relation to the other closely-related species of Macaca.^*This paper is dedicated to Dr. A. J. T. Johnsingh for his immense contributions to the study and conservation of India’s wildlife and for being an inspiration to a whole generation of students.     

Mother-infant relationships in bonnet macaques: Sources of variation in proximity

Family composition is an important predictor of variation in proximity among captive bonnet macaque (Macaca radiata) mothers and their infants. Infants that have several immature sisters in the group are initially more independent that infants with fewer sisters, but as they reach 6 months of age infants with several sisters become less independent than their peers. The effects of the presence of juvenile females on the relative independence of their infant siblings seem to be related to the fact that the members of families with several immature females are the targets of more aggression than are the members of other families.     

How social relationships influence a monkey's choice of feeding sites in the troop of Japanese macaques (Macaca fuscata fuscata) on Koshima islet

When the individual Japanese macaques of the Koshima troop feed on natural food, they usually feed alone. In situations where animals usually feed without other animals, there is a possibility that subordinate animals may avoid feeding sites at which dominant animals are feeding. This paper examines whether social relationships such as kinship or dominance exert any influence on an animal's choice of feeding sites, by analyzing episodes in which an animal approached and climbed into a tree where other animals were. As a result, it was found that social relationships did not influence whether an animal climbed into a tree where other animals were feeding, and that no particular age-sex pair co-fed. Agonistic interactions frequently occurred when the inter-individual distance was less than 1 m. From these findings, the feeding sites were divided into two spaces: (1) a tolerance feeding space, and (2) an intolerance feeding space. It is presumed that animals can feed without entering others' intolerance feeding spaces when food is abundant, as it was in the present study period. Thus social relationships do not influence an animal's choice of feeding sites in such a situation.     

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.     

Observation of a birth among wild toque macaques (Macaca sinica)

Most toque macaques give birth to their infants during the night when resting arboreally. Here we report on a birth that occurred in daytime (at 0916 hr) and on the ground. The mother was 7.6 years old; the birth was her second. Prepartum behaviors included lordosis, arching of the back, stretching, squatting, rolling on the ground, and anogenital self-examination. During the birth the female was isolated about 100 m from the rest of her group. The mother stood bipedally during parturition and assisted delivery with her hands. The infant was born within 2 min after first appearing at the vulva. It immediately clung to the mother’s leg and vocalized. The mother licked the infant and oriented it toward her ventrum. She resumed foraging behavior within 20 min after parturition. The infant nursed for the first time 2.25 hr after being born. The mother ate part of the placenta, but the alpha female of the group usurped and also ate a portion of it. Curious group members sniffed and looked at the infant but did not touch it.     

Early mother-infant relationships ofMacaca thibetana at Mt. Emei China

Quantitative data on early mother-infant relationships in the Tibetan macaque was collected during the first 23 weeks of infant life in spring, 1987, at Mt. Emei, China. During the first week of life, infants spent 98.3% of their time in ventroventral contact with their mothers. This contact rapidly decreased to 33.8% by the 4th week and thereafter to 0.85% by the 23rd week. Nipple contact decreased relatively slowly from 89.7% to 62.9% within the first 4 weeks of infant life and to 19.8% by the 23rd week. Ventrolateral and ventrodorsal contact appeared by the 2nd week, meanwhile, maternal restraining behavior appeared, and reached a peak by the 3rd week. The mother neither encouraged nor discouraged her infant's independence during 4–8th weeks. Maternal rejection of the infant was first observed when the infant was 11 weeks old and continued thereafter.