Synchrony of estrous swelling in captive group-living chimpanzees (Pan troglodytes)

Recent findings suggest that menstrual synchrony may occur in humans and is more dependent on factors of close personal association than simple prox imity. Part I of this study analyzed the estrous cycles of 10 captive group living chimpanzees (Pan troglodytes) housed in two separate groups in the same building. Each group contained at least one male. The mean discrepan cies for (1) the approximate day of ovulation (last day of maximum swelling) and (2) the day of onset of estrous swelling were determined for all possible pairs within groups and compared to the mean discrepancies of pairs between groups. With respect to the probable day of ovulation, the mean discrepancy of animals caged together was 8.0 days and that of animals caged separately was 10. 7 days. Comparing the onset of estrous swelling, the mean between groups was 10.4 days, whereas females caged together averaged only 5.7 days. A repeated-measures analysis of variance indicated a significant group effect in the onset of estrous swelling (F = 5.68,p < 0.05), whereas there was no significant difference between the animals caged together and those caged separately with respect to the last day of maximum swelling (F = 1.37, NS). Part II of the study compared the onset of the first postpar tum estrus (PPE) to the onset of estrus in cagemates. During a 6-year period, 13 females exhibited 33 PPEs while in social contact with cycling females. Of 86 paired comparisons, the PPE onset of 43 (50%) occurred with in 6 days of the swelling onset of a cagemate. The results suggest that, as in other species (including humans), the social contact and time spent together influence the synchrony of chimpanzee estrous cycles, especially in terms of swelling onset. The synchrony of estrous swelling and possible mediation by olfactory and/or hormonal cues are discussed as they relate to chimpanzee social structure and female reproductive strategy.     

Dynamics of Estrous Synchrony in Captive Gray Mouse Lemurs (Microcebus murinus)

Estrous synchrony in seasonal breeders can in principle be based on and shaped by environmental, internal, and/or social cues. We analyzed the dynamics of estrous synchrony for the first time in a seasonal, nocturnal primate species, the gray mouse lemur (Microcebus murinus). We compared successive estrous cycles and different levels of spatial proximity over two reproductive seasons in a captive population in order to identify possible social influences on estrous synchrony. The females exhibited a marked estrous synchrony at the beginning of each reproductive season, but we found no indication of a process of socially induced synchronization among them. Females housed in the same cage/room were not more strongly synchronized than females housed in different cages/rooms. Moreover, cycles desynchronized from the first to the second estrus of the season. Estrous cycle length did not depend on age, parity, or social housing conditions, but instead mainly on the individuality of the lemurs. This individuality, shown for the first time in a nocturnal primate species, is likely to be based on an endogenous rhythm with a genetic basis. We discuss possible social advantages, e.g., communal rearing, and disadvantages, e.g., mate choice and female-female competition, of estrous synchrony for nocturnal primates living in a dispersed individualized social network, and propose that a moderate flexibility within the individual cycle lengths probably enables the females to compromise between the different socioecological pressures.     

Reproductive Schedules of Female <Emphasis Type="Italic">Microcebus rufus</Emphasis> at Ranomafana National Park,Madagascar

I examined the reproductive status of female brown mouse lemurs (Microcebus rufus) from October 2005 to early January, 2006 at Ranomafana National Park, an eastern rain forest in Madagascar. I employed intensive capture/mark/recapture techniques to track individual changes in vaginal morphology and body mass and collected vaginal smears for individuals with open vaginas. I observed moderate estrous synchrony (vaginal openings between October 11 and November 18), with clusters of females showing strong estrous synchrony (6 of 15 on or around October 15, and 3 of 15 on or around October 25). My findings weakly support the proximity hypothesis—that closer females will enter estrus simultaneously—and offer virtually no support for the notion that body mass influences the timing of estrus in brown mouse lemurs. Females gave birth during the second and third weeks of December. Two females showing signs of abortion or perinatal death of offspring also showed renewed vaginal swelling in late December, suggesting that some form of polyestry, i.e., as reproductive compensation for infant loss, exists at Ranomafana. I discuss the implications of the data, in conjunction with other evidence of polyestry in wild mouse lemurs, in light of data on patterns of seasonality at Ranomafana and other sites. More data are needed to determine the frequency and pattern of polyestry in Microcebus rufus.     

Menstrual synchrony

Several studies have now documented menstrual synchrony in human females. There is a broad consensus that the phenomenon mainly occurs in women who spend a significant amount of time together, such as close friends and coworkers, and that social contact rather than a similar environment plays an important role in mediating the effect. However, the mechanisms involved and the adaptive function of menstrual synchrony are not understood. There is some evidence that olfactory cues between females might underlie the effect. More research is needed before the precise mechanisms that regulate menstrual synchrony are elucidated. Cynthia Graham received her MSc in clinical psychology from Glasgow University and her PhD from McGill University. Her previous research has involved menstrual synchrony and the effects of oral contraceptives on premenstrual changes. Currently she is working on a World Health Organization project assessing the effects of steroidal contraceptives on well-being and sexuality.     

Menstrual synchrony: Fact or artifact?

Although more than thirty years of intensive investigation have passed since McClintock first published results on menstrual synchrony, there is still no conclusive evidence for the existence of this phenomenon. Indeed, a growing body of nullresult studies, critiques of menstrual synchrony studies, and the lack of convincing evolutionary explanations bring into question the existence of this phenomenon. This paper presents results of a study conducted over five consecutive months in Polish student dormitories. In 18 pairs and 21 triples of college-age women, menstrual synchrony was not found. Social interactions, considered the most important factor mediating the effect of menstrual synchrony, was unrelated to any difference in menstrual cycle onsets. Initial menstrual onset difference was influenced by woman’s body mass and menstrual cycle irregularity. These results provide further evidence that women do not synchronize their menstrual cycles.     

Estrous synchrony in a group of African elephants (Loxodonta africana) under human care

Synchrony of estrous, and consequently of conception and birth of young, may be of adaptive significance for certain mammals. Among the species in which estrous synchrony has been suspected several times are elephants, but clear evidence is still missing. We determined estrous cycles of African elephants (Loxodonta africana) (n=4) at the Vienna Zoo, Austria, between June 2003 and January 2006 by measuring serum progesterone levels from weekly blood samples. Except for the dominant female when she was intensively lactating, all animals showed clear cycles or progesterone release with a mean period of 105.3+/-15.37 days. For most of the study period, estrous cycles were asynchronous between females. However, after re-occurrence of the progesterone cycle in the dominant female following the first period of lactation, all four females showed high synchrony of progesterone release over the two subsequent cycles. Large changes in individual period lengths indicated that synchronization was due to the adjustment of cycle length in subdominants to that of the dominant female. We used a bootstrap procedure, based on resampling measured times of progesterone peaks, to determine if this apparent synchrony could have been caused by chance alone. This statistical analysis indicated that between-individual variances of the timing of progesterone peaks were much smaller that to be expected by chance (P=0.009). This finding represents the first evidence for estrous synchrony between elephants. We discuss various hypotheses to explain the biological function of cycle synchrony in elephants.     

Determinants of behavioral rhythmicity during artificial menstrual cycles in rhesus monkeys (Macaca mulatta)

Reproductive success in many mammals depends on synchrony between copulation and ovulation, which is insured by the phenomenon of heat in the female. Certain anthropoid primates including rhesus monkeys do not show heat but may copulate throughout the menstrual cycle, especially when pairs are isolated from conspecifics. In social groups, however, mating mostly occurs around midcycle. We wished to test the hypothesis that copulations are more closely linked to ovulation when males have simultaneous access to several females in different cycle phases. Artificial menstrual cycles were therefore induced by giving hormones to ovariectomized female rhesus monkeys observed in small social groups that each consisted of four females and one male. The cycles of two hormone-treated femlab in each group were either made to synchronize or be offset by 7-day increments so that the estradiol peak of one female occurred 7 days before, and 7 and 14 days after, the estradiol peak of the other. Radioimmunoassay of plasma samples (N = 224) confirmed the timing of the estradiol peaks. Results from eight unique male-female groups (4 males, 8 females, 16 male-female pairs, 718 tests) fully supported the hypothesis. Compared with synchronized cycles, the amplitudes of rhythmic changes in offset cycles were reduced for ejaculations made by males but greatly enhanced for ejaculations received by females. We propose that this socio-hormonal integration of behavior in the group is highly adaptive and enhances the reproductive success of both males and females.     

You mate, I mate: macaque females synchronize sex not cycles

Extended female sexuality in species living in multimale-multifemale groups appears to enhance benefits from multiple males. Mating with many males, however, requires a low female monopolizability, which is affected by the spatiotemporal distribution of receptive females. Ovarian cycle synchrony potentially promotes overlapping receptivity if fertile and receptive periods are tightly linked. In primates, however, mating is often decoupled from hormonal control, hence reducing the need for synchronizing ovarian events. Here, we test the alternative hypothesis that females behaviorally coordinate their receptivity while simultaneously investigating ovarian cycle synchrony in wild, seasonal Assamese macaques (Macaca assamensis), a promiscuous species with extremely extended female sexuality. Using fecal hormone analysis to assess ovarian activity we show that fertile phases are randomly distributed, and that dyadic spatial proximity does not affect their distribution. We present evidence for mating synchrony, i.e., the occurrence of the females' receptivity was significantly associated with the proportion of other females mating on a given day. Our results suggest social facilitation of mating synchrony, which explains (i) the high number of simultaneously receptive females, and (ii) the low male mating skew in this species. Active mating synchronization may serve to enhance the benefits of extended female sexuality, and may proximately explain its patterning and maintenance.     

Social dominance determines estrous entrainment among female hamsters

In order to study the phenomenon of estrous entrainment and its relation to social behavior two studies were conducted with female hamsters. In the first experiment single females were placed in close proximity, but not in direct contact with three other females whose estrous cycles were already synchronous. The single female was either in phase (control) or out of phase (experimental) with the synchronous females. In the second experiment two females at the same (control) or different (experimental) points in their estrous cycles lived together until entrainment occurred. Their social interactions during the initial 30 min in this shared habitat were observed and a dominance hierarchy established. Estrous stage was determined daily for each animal by vaginal lavage. The major findings of these studies are (1) estrous entrainment occurred in all female hamsters whether living in close proximity (Expt I), or living together (Expt II); (2) regardless of the stage of estrous at the start of cohabitation, hamsters' cycles may be either accelerated or decelerated depending on whether the partner's stage is ahead or behind their own; (3) social interaction appears to accelerate the entrainment process, and (4) when examined in light of social dominance, the behaviorally submissive animals entrained to the behaviorally dominant animals.     

Human axillary secretions influence women''s menstrual cycles: The role of donor extract of females

Menstrual synchrony in human females has previously been demonstrated among women attending a predominantly female university as well as among women attending coeducational universities. In each of these studies, women who spent the most time together were most likely to show the menstrual synchrony. In this experiment, the possibility that substances in axillary secretions might mediate this effect was tested using a prospective, double-blind research design and a combined axillary extract from a group of female donors. Female subjects who reported themselves to have normal (29.5 +/- 3 day) cycles were exposed to the axillary extracts or blank/ethanol for 10 to 13 weeks. Recipients of the axillary extracts showed a significant reduction in "days' difference in menses onset" relative to the donor cycle, no change was evident for recipients of blank/ethanol. These results demonstrate that constituents from the axillary region of donor females can shift the time of menstrual onset of another group to conform with the donors' cycle and that this effect can occur even in the absence of social contact.     

圈养马麝(Moschus sifanicus)发情交配节律的比较研究

在1997～2000年间,甘肃兴隆山麝场的圈养马麝发情交配的时间节律保持相对年间恒定,1996年麝场进行了大规模的圈群间动物调整,导致该年的马麝圈群进入发情较迟,发情持续时间也较其他年份长。总体上,圈养马麝的发情持续时间达3个月,而66％的的发情交配发生于1个月内（从11月21日～12月21日）,发情季节（75％的发情完成累计时间）长36天。雌性圈养马麝发情的时间格局受圈养环境的季节性因子影响。饲养人员的饲养风格及各个饲养区内雌性马麝的社会行为的调节效应,各饲养区动物的发情时间格局有显著差异。年龄可影响马麝的发情交配,5．5岁龄以上的马麝发情定时更早。上一年度的繁殖成功与否和当年动物发情迟早无显著相关。野捕圈养麝群和其F1代圈群间的发情时间格局无显著差异。有较多发情周期的个体并不比发情周期仅1～2次的个体更早进入发情。     

Social structures in Pan paniscus: testing the female bonding hypothesis

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male–female or male–male dyads. We also investigated five mother–son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.     

Timely estrus in wild brown mouse lemur females at Ranomafana National Park, southeastern Madagascar

The small-bodied nocturnal mouse lemurs (genus Microcebus) occupy a variety of habitats in Madagascar. Gray (M. murinus) and brown (M. rufus) mouse lemurs have been widely studied both in the wild and captivity. Whereas captive studies revealed an endogenous regulation of reproduction entrained by photoperiod, field studies have suggested that reproductive activation could be affected by additional climatic, physical, or social conditions. I collected data on wild brown mouse lemur females at Ranomafana between 2004 and 2008 to determine: 1) the timing of estrus and estrous periodicities across multiple seasons, and 2) whether additional factors such as body mass, age, or rainfall are correlated with onset of reproduction. In mouse lemur females at Ranomafana, the first seasonal estrus occurs 3-4 weeks after the vernal equinox. I report ~1 month's intra-population variation in the timing of estrus and inter-annual estrous intervals with periodicities of ~365 days. There were significant differences between the onset of reproduction across years. Estrous onset was uncorrelated with body mass, but there was an apparent age effect. There was a significant negative correlation between August rainfall and onset of reproduction when 2004 data were removed from the analysis. Results from this study are consistent with the notion that timing of estrus is photoperiod-dependent. As in captivity, intra-population variation in estrous onset is ~4 weeks in length. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments.     

Mating stimulation required for mating-induced estrous abbreviation in female rats: effects of repeated testing

Mating stimulation, particularly vaginal-cervical stimulation, causes estrous abbreviation in female rats. In most previous studies, female rats were repeatedly tested for sexual behavior until estrous termination occurred. Thus, it was not clear whether sensory stimulation (e.g., flank stimulation, olfactory cues) received during the repeated testing procedure contributed to estrous abbreviation. In Experiment 1, we determined the effect of premating to two or four ejaculations on the rate of estrous termination when a repeated testing procedure was used. We compared ovariectomized, hormone-primed, female rats receiving (1) four ejaculations, (2) two ejaculations, or (3) no premating. Females premated to either two or four ejaculations showed significantly lower levels of sexual receptivity 12 h later than did nonpremated females. These results confirm that premating induces estrous abbreviation when a repeated testing procedure is used. In Experiment 2, we determined whether the repeated testing procedure was necessary for estrous abbreviation. Ovariectomized, hormone-primed female rats were premated to two ejaculations or not premated. The rats were then tested for sexual behavior repeatedly or only once. Females that were premated and repeatedly tested for sexual behavior showed a statistically significant decrease in sexual receptivity compared to females that were not premated; however, the level of sexual receptivity in premated females did not differ from that in non-premated females when they were tested only once. The results suggest that heat duration is the result of a complex interplay between those factors that promote the expression of sexual receptivity and those that inhibit it.     

A new method for evaluating flowering synchrony to support the temporal isolation of genetically modified crops from their wild relatives

Hybridization between crops and their wild relatives potentially threatens the genetic identity of the wild plants, particularly in the case of genetically modified crops. Only a few studies have examined the use of temporal isolation to prevent hybridization, and the indices used in those studies, (e.g., the days of flowering overlap), are not precise to evaluate the degree of synchrony in flowering. Here we propose a flowering similarity index that can compare the degree of flowering synchrony between two relevant species and measure the efficiency of temporal isolation. The results showed that the flowering similarity index predicts the likelihood of hybridization much better than the number of flowering-overlap days, regardless of different flowering patterns among cultivars. Thus, temporal isolation of flowering or flowering asynchrony is the most effective means in preventing hybridization between crops and their wild relatives.     

Sexual initiation in wild mountain gorillas

A field study of wild mountain gorillas was conducted to elucidate details of sexual initiation required for an interpretation of the increased frequency of copulation during the menstrual cycle, in comparison to the wild, that occurs when this species is tested in traditional laboratory pair tests. Although females in the wild played a clear role in establishing and maintaining proximity to the male and assertively presenting for copulation, all female presenting was preceded by some form of behavior by the male. Of particular relevance were several components of the male’s chest-beat display that had been observed at much higher frequencies in the laboratory tests. Although originally described as male aggression in the laboratory tests, such behavior now appears to be male sexual initiative, elicited by female proximity. The exaggerated form and frequency of the display in the laboratory, and the increased copulation during the cycle that ensued, are likely due to (1) placing females in proximity to a male daily, rather than on 2–3 days of estrus as occurs in the wild, and (2) the inability of the female in the laboratory to withdraw from male proximity during pair tests in a single cage. In addition to clarifying the data on laboratory pair tests, the data on wild gorillas have relevance to the captive breeding of gorillas.     

Effects of the distribution of female primates on the number of males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups.     

Sexual preferences during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

Eight groups of rhesus monkeys each consisting of one male and four ovariectomized females were observed while two of the females were treated with hormones to produce artificial menstrual cycles. These were either synchronized or offset by 7-day increments. Sexually preferred females, defined by the numbers of ejaculations per test, received almost twice as many ejaculations as did non-preferred females during all synchronized and offset cycles and during all cycle phases. However, short-term changes in partner preference occurred when the midcycle phase of non-preferred females coincided with the middle or late progesterone phase of preferred females, suggesting a negative effect of progesterone on behavior during the menstrual cycle. There were highly significant differences between preferred and non-preferred partners for almost all of their sexual and social interactions, and preferred partners showed longer proximity and grooming times as well as higher levels of sexual activity. Partner preferences accounted for more of the behavioral variance between pairs than did female dominance, although males sought the proximity of dominant females independently of their partner preferences. Thus, in a setting uncomplicated by male mate competition, sexual preference by male rhesus monkeys is a robust phenomenon depending on complex interactions between dominance, hormonal status, and the individual behavior of female partners.     

Sampling scale can cause bias in positive assortative mating estimates: evidence from two intertidal snails

Assortative mating in the wild is commonly estimated by correlating between traits in mating pairs (e.g. the size of males and females). Unfortunately, such an approach may suffer from considerable sampling bias when the distribution of different expressions of a trait in the wild is nonrandom (e.g. when segregation of different size classes of individuals occurs in different microhabitats or areas). Consequently, any observed trait correlation in the wild can be an artefact of pooling heterogeneous samples of mating pairs from different microhabitats or areas rather than true nonrandom matings. This bias in estimating trait correlations as a result of sampling scale is termed the scale‐of‐choice effect (SCE). In the present study, we use two intertidal littorinid species from Hong Kong to show how the SCE can bias size‐assortative mating estimates from mating pairs captured in the wild, empirically demonstrating the influence of this effect on measures of positive assortative mating. This finding cautions that studies overlooking the SCE may have misinterpreted the magnitude and the cause of assortative mating, and we provide a new analytical approach for protecting against this potential bias in future studies.     

Mechanisms of social synchrony between circadian activity rhythms in cohabiting marmosets

In marmosets, social synchrony between circadian profiles of activity is stronger in animals that cohabit in a family. The activity of three breeding pairs was recorded by actiwatches to investigate the mechanisms involved in the synchrony between the circadian activity profiles during cohabitation in marmoset reproductive pairs. The dyads were submitted to LD 12:12 (21 days) and LL: 1) cohabitation (24 days), 2) removal of the cage mate (20 days), 3) reintroduction of the mate into the cage of the 1^st situation (30 days) and 4) removal of the cage mate (7 days). Next, they were rejoined and maintained in LD 12:12 (11 days). In conditions involving cohabitation of pair, the general and maximum correlation indexes between circadian profiles were higher in cage mates compared to animals of the same or different sex with which they maintain only acoustic and olfactive contact. This strong synchrony between rhythms was accompanied by a stable phase relationship at the activity onset and offset, with identical circadian periods between mates. When the pairs were separated, there was a break in stability in the phase relationships between activity profiles with different circadian periods and a greater phase angle difference between rhythms of cage mates. During separation, two females and one male progressively anticipated the activity onset and offset in a phase similar to that in previous conditions, expressing entrainment to the mate. During the first reintroduction, two pairs exhibited signs of masking in rhythm. Although modulation in the rhythm of some animals has been observed through acoustic cues from animals outside the colony, we suggest that cohabitation favors strong synchrony between the circadian activity profiles of marmoset reproductive pairs involving synchronization by entrainment and masking. Further studies in the absence of external social cues are necessary to clarify the role of these mechanisms on social synchronization in marmosets.