Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys,Brachyteles arachnoides

The analysis of fecal ovarian steroids provides a powerful noninvasive method to obtain insights into ovulatory cycles, gestation length, and the timing of sexual interactions relative to the periovulatory period in wild primates. Techniques developed to collect and assay feces from free-ranging muriqui monkeys (Brachyteles arachnoides) for estradiol and progesterone yield the first explicit reproductive data on this species, and provide the first opportunity to evaluate the timing of observed copulations with muriqui ovarian cycles. Hormonal profiles from seven females indicate average cycle lengths of 21.0 ± 5.4 days (n=20). Females conceived after 3–6 ovulatory cycles. Gestation length averaged 216.4 ± 1.5 days for the five females for which conception cycles were sampled. Discrete copulation periods spanned an average of 2.1 ± 1.2 days (n=29), with intervals between these concentrated periods of copulations averaging 15.6 ± 6.7 days (n=20). There were no significant differences among females in cycle lengths, copulation period lengths, or copulation interval lengths. Ejaculation was visible following 71.8 ± 26.7% of copulations during the females' preovulatory periods. All females copulated outside the periovulatory period. The proportion of copulation days outside the periovulatory period was slightly greater (p=0.08) for primiparous females (64.8 ± 28.3%) than for multiparous females (28.7 ± 19.7%). Am. J. Primatol. 42:299–310, 1997. © 1997 Wiley-Liss, Inc.     

Assessment of circadian rhythms throughout the menstrual cycle of female rhesus monkeys

Reproductive cyclicity has a significant influence on the regulation of circadian rhythms in rodents. Studies have suggested that there are changes in body temperature rhythms between the follicular and luteal phases in human females. This study examined the effects of menstrual cyclicity on physiological and behavioral circadian rhythms in female rhesus monkeys (Macaca mulatta), an acknowledged biomedical model. Seven unrestrained subjects were implanted with a biotelemetry transmitter to measure body temperature and heart rate and an accelerometer was used to measure physical activity. Water was available ad libitum and drinking was measured via an electronic circuit attached to a water lixit. A video-based task system, the Psychomotor Test System, provided environmental enrichment and delivered a pelletized diet. Mean, phase, and amplitude of each rhythm were calculated. Estrogen and progesterone conjugates were assayed and quantified from daily urine samples to identify follicular and luteal phases of the menstrual cycle. Average circadian variables were then compared between these phases. Heart rate was significantly (P< or =0.05) delayed in the luteal phase. Albeit non-significant, analysis showed a trend toward decreased circadian amplitude of body temperature in the luteal phase.     

Juggling priorities: female mating tactics in Phayre's leaf monkeys

Extended sexual receptivity in primates is thought to facilitate paternity confusion, thus decreasing the risk of infanticide. However, females might also provide some indication of ovulation to attract preferred males during fertile periods. We examined female mate preferences across defined receptive periods (N = 59) in a group of wild Phayre's leaf monkeys (Trachypithecus phayrei crepusculus) at Phu Khieo Wildlife Sanctuary (February-September 2006; 2,603 contact hours). The group contained seven cycling adult females and three reproductively active males (one adult and two adolescents). We predicted that females would prefer the adult male during periovulatory (POP) receptive periods, but the adolescent males during nonperiovulatory (NPOP) and postconceptive (PC) periods. We collected focal and ad libitum data on sexual and agonistic behaviors to determine female preferences and male awareness of female fertility. We also determined the degree of mating overlap to assess if males were capable of monopolizing females. Our results indicate that females were more frequently proceptive and receptive toward the adult male during POP. By contrast, females were more proceptive and receptive toward one of the adolescent males during PC periods, but rarely interacted with the other adolescent. Patterns of attractivity and agonism across receptive periods suggested that the adult male could detect fertility, while the preferred adolescent could not. Finally, we found a high degree of overlap in total receptive period days, but a low degree of overlap in POP receptive days, suggesting that the adult male might have monopolized females, especially since he seemed to be aware of female fertility. Although these results suggest that females provide some information on ovulation, they also suggest that females attempt to confuse paternity, perhaps capitalizing on male differences in the ability to detect fertility.     

Agonistic behavior and dominance relationships in female Phayre's leaf monkeys -- preliminary results

Socioecological theory suggests a link between the strength of competition for food/safety, rates of agonism, structure of dominance hierarchies, and dispersal among group-living females. This study presents preliminary data on agonistic behavior and dominance relationships for female Phayre's leaf monkeys (Trachypithecus phayrei), a species in which females routinely disperse. Behavioral observations were conducted on two groups (four adult females, and five adult females plus two juvenile females, respectively) at Phu Khieo Wildlife Sanctuary, northeast Thailand. Rates of agonistic behavior were analyzed from focal continuous recordings, while dominance hierarchies were constructed from all agonistic behaviors (focal and ad libitum sampling). Overall, female-female agonistic behaviors (aggression, submission, and displacements) occurred at a rate of < 0.25 interactions per hour. Agonistic interactions involving food occurred more frequently than expected based on feeding time. Females in both groups exhibited linear dominance hierarchies with some reversals, and possibly an age-inversed hierarchical structure in the larger group. The results fit well with previous results for colobine monkeys regarding frequency of interactions, displacements predominating agonistic behavior, and the possibility of an age-inversed hierarchy. The results contradict the suggested link between linearity of hierarchies and female philopatry. Future studies should consider the notion that female dispersal may coexist with linear dominance hierarchies.     

Reproductive performance of a laboratory breeding colony of patas monkeys (Erythrocebus patas)

Reproductive statistics were gathered over a 5½-year period on a colony of Erythrocebus patas. Pregnancies occurred throughout the year under laboratory conditions with a suggestion of a mating peak in the late fall and early winter. Menstrual cycles were monitored and found to average 30.6 days in length. Maximal vaginal cornification occured on day 15 of the cycle suggesting a midcycle ovulation. However, production of timed-mated pregnancies indicated ovulation occurred earlier and that breeding on days 10, 11, and 12 after menstruation was more likely to result in pregnancy. The gestation length was found to average 167.2 days in 142 harem-bred females and 167.5 days in 11 timed-mated pregnancies. Sixty-two percent of all pregnancies resulted in live births; 28% of the conceptions terminated with in-utero death of the fetus. Stillborn infants were delivered in 9% of the pregnancies. Infant mortality during the first 6 months of life was 10.2%. Females raised in the colony conceived their first offspring at approximately 3 years of age and males were able to sire infants at 3 years and 8 months.     

The meaning of weaning in wild Phayre's leaf monkeys: Last nipple contact,survival, and independence

In primates and other mammals, weaning is an equivocal concept, as is reflected in the numerous ways it is measured: a) first intake of solid food, b) conflict over access to the nipple, c) ability to survive without mother, d) maternal resumption of cycling, or e) the cessation of nipple contact. The lack of a consistent definition means that weaning age, although it falls between gestation (fetal growth) and age at first reproduction (most energy diverted from growth), is currently not a reliable life history variable capturing offspring independence. Using data for wild Phayre's leaf monkeys (Trachypithecus phayrei crepusculus) at Phu Khieo Wildlife Sanctuary, Thailand (51 offspring, four groups), we asked whether the end of nipple contact indicates offspring independence as measured by survival to 3 years. To establish a baseline for the onset of independence, we assessed the youngest age at which individuals were orphaned (15–17 months) but then survived to 3 years. Next we determined that offspring age at last nipple contact (19.0 months) was comparable to two other independently calculated measures: offspring age at mother's first postpartum ovulation (11.5 months), and age at mother's re‐conception (15.6 months). Using these separate “starting points,” we arrived at similar ages for nipple contact cessation (18.4 and 19.2 months, respectively). Overall, in wild (but not in provisioned) Asian colobines, age at last nipple contact was allometrically related to adult female body mass, supporting its designation as a life history variable. Future comparisons need to show if this holds for other taxa. Am J Phys Anthropol 154:291–301, 2014. © 2014 Wiley Periodicals, Inc.     

Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys

In many primates species, female sexual attractivity is influenced by behavioral cues as well as by nonbehavioral cues (i.e., visual-morphological or chemical signals). Both kinds of cues are usually related to the ovarian cycle and female hormonal state. Female tufted capuchins (Cebus apella) lack any external morphological change in relation to the ovarian cycle and evidence of scent-marking behavior has never been reported. In addition, tufted capuchin males do not routinely investigate the female's body or urine. Instead, capuchin females are extremely active in sexually soliciting the male(s) and their courtship toward them involves a rich behavioral repertoire. In the present study we defined female tufted capuchin proceptivity and investigated its relationship with female reproductive state. Ovarian hormones were measured in urine and fecal samples from four captive females in order to (a) assess their reliability for monitoring female ovarian function and (b) provide information on the timing of the component cycle phases and in particular the periovulatory phase. Measurements of urinary and fecal progestin metabolites provided the best indicator of ovarian cyclicity and for timing of the periovulatory phase. Through a multivariate analysis of the behavioral data set we distinguished four behaviors (eyebrow raising with vocalization, touching-and-running, nuzzling and head cocking) which showed a marked cyclicity (21.3 days) that matched that of urinary progesterone (21.9 days). Data showed that each period of proceptive behaviors was 2.7 +/- 0.8 days long and the day of a defined luteal phase rise in urinary progesterone levels was markedly shifted toward the end of this period. Furthermore, the ejaculations observed always occurred within proceptive periods. The results clearly indicate that female behavior is a good indicator of the periovulatory phase and can enhance female attractivity.     

Fecal analysis of ovarian cycles in female black-handed spider monkeys (Ateles geoffroyi)

An enzyme immunoassay (EIA) was applied to characterize the reproductive endocrinology of adult female black-handed spider monkeys (Ateles geoffroyi). Analysis of paired urine and fecal samples, collected from two females housed at San Diego Zoo, confirmed that the EIAs employed provided quantitative measurements of ovarian sex steroid hormones. Fecal metabolite levels were significantly correlated with those in urine, confirming that feces are a valid source of steroid metabolites in this species. The excretion of these metabolites in feces lagged urinary excretion by 1-2 days. The ovarian cycle profiles of the two captive females and five free-ranging females are comparable, with an average length of approximately 20-23 days. Cyclical bleeding, as previously reported, was observed in one of the two captive females. Pregnancy was detected in four free-ranging females, and early fetal loss for one female was indicated by hormonal data.     

Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata)

In this study we investigated the reproductive characteristics of wild female Japanese macaques (Macaca fuscata fuscata) in 2 nonconsecutive years using noninvasive methods to monitor physiological events. We detected ovulation dates and ascertained conceptions from fecal hormone profiles. First ovulations occurred from middle October to early November in 1997, and from middle to late November in 1999. Most females conceived during their first ovarian cycle. On average, postconception bleeding occurred 18.4 days after ovulation, and menstruation occurred 13.7 days after ovulation. The average gestation length was 176.3 days. The average degree of facial redness and the percentage of females that copulated synchronously changed across the ovarian cycle and peaked in the periovulatory period. Although prolonged periods of postconception copulation have been reported in previous studies, they did not occur in this study, which suggests that such behavior may not be a species-typical characteristic. Female fertility varied between the 2 years. The copulation rates of females with no infant <1 year of age were 100% (14/14) in 1997 and 45.5% (5/11) in 1999. The ovulation rates of the female subjects that we chose for hormonal assays were 100% (9/9) in 1997 and 50.0% (3/6) in 1999. Th conception rates of these selected females were 100% (9/9) in 1997 and 16.7% (1/6) in 1999. The birth rates (the number of females that delivered divided by the total number of adult females in the troop) were 73.3% (11/15) in 1998 and 6.7% (1/15) in 2000. The modified birth rates (the number of females that delivered /the number of adult females with no infant <1 year of age) x 100 were 78.6% (11/14) in 1998 and 9.1% (1/11) in 2000.     

Reproductive biology of captive alpine ibex (Capra i. ibex)

We studied the reproductive biology of alpine ibex bred at the Peter & Paul Wildlife Park, St. Gallen, Switzerland, from 1930 through 1943 and 1968 through 1983. Peter & Paul Wildlife Park had supplied most of the original stock used to reestablish ibex populations in the European Alps after they had become extinct. Ibex females were seasonally polyestrous. Their estrous cycle averaged 20 days, and their gestation period averaged 167 days. Females between 1 and 15 years of age on average produced 0.78 young per year; females between 3 and 13 years of age produced 0.99 young per year. The average age at which captive ibex females gave birth was 8.44 years. Sex ratio at birth was unbiased. More singletons than twins were born, but the proportion of twins born during the years 1968 through 1983 was higher than during the earlier study period. There were no differences in the survival rates of male or female and single or twin offspring.     

Circadian profiles of progesterone,gonadotropins, cortisol and corticotropin in cycling and postmenopausal women

Little is known about the regulation of temporal variations of progesterone over the 24-hr span in young cycling women as well as in postmenopausal women. The purpose of the present study was to investigate the relationships between diurnal variations of progesterone and diurnal variations of hormones of the gonadotropic and corticotropic axes, and to provide further information on the source of progesterone secretion under physiological conditions. Twenty-four-hour hormonal profiles were explored under well-controlled laboratory conditions in 10 healthy women (21–36 yr old) with normal ovulatory cycles during early-mid follicular and late luteal phases, and in 8 healthy postmenopausal women (48–74 yr old). In young cycling women, significant positive relationships were found between progesterone and follicle-stimulating hormone (FSH) – but not luteinizing hormone (LH) – profiles during late luteal phase. Conversely, during follicular phase, significant positive relationships were evidenced between progesterone and cortisol profiles, but not between progesterone and FSH or LH. In postmenopausal women, strong positive correlations were found between progesterone and corticotropin (ACTH) or cortisol profiles. The present results indicate that during late luteal phase, temporal progesterone profiles are associated with FSH rather than with LH profiles. They also provide evidence that adrenal cortex is a major – or possibly the only – source of progesterone production during the follicular phase of the normal ovulatory cycle, and probably the only source after menopause.     

Estrous state influences on investigative,aggressive, and tail flicking behavior in captive female Asian elephants

Females of species that live in matrilineal hierarchies may compete for temporally limited resources, yet maintain social harmony to facilitate cohesion. The relative degree of aggressive and nonaggressive interactions may depend on the reproductive condition of sender and receiver. Individuals can benefit by clearly signaling and detecting reproductive condition. Asian elephants (Elephas maximus) live in social matrilineal herds. Females have long estrous cycles (14–16 weeks) composed of luteal (8–12 weeks) and follicular (4–8 weeks) phases. In this study, we observed the behavior of four captive Asian elephant females during multiple estrous cycles over 2 years. We evaluated whether investigative, aggressive, and tail flicking behaviors were related to reproductive condition. Investigative trunk tip contacts showed no distinct pattern by senders, but were more prevalent toward female elephants that were in their follicular compared with their luteal phase. The genital area was the most frequently contacted region and may release reproductively related chemosignals. Aggression did not differ significantly with estrus; however, rates of aggression were elevated when senders were approaching ovulation and receivers were in the luteal phase. Females in the follicular phase may honestly advertise their condition. Contacts by conspecifics may serve to assess condition and reduce aggression. A behavior termed “tail flicking” was performed mainly during the mid‐follicular phase when estrogen and luteinizing hormone levels are known to spike. Tail flicking may disperse chemical signals in urine or mucus as well as act as a tonic signal that could provide a means of anticipating forthcoming ovulation by elephants and also for human observers and caretakers. Zoo Biol 27:167–180, 2008. © 2008 Wiley‐Liss, Inc.     

Reproductive parameters of wild female Rhinopithecus roxellana

On the basis on 6 years of observation, we estimated the reproductive parameters of a Golden snub-nosed monkey (Rhinopithecus roxellana) group in the Qinling Mountains, China. We observed 88 births in 47 females from 2001 to 2006. Two methods were used to calculate the birthrate. The first method is based on the number of births observed in a year, giving 0.49+/-0.07 (mean+/-SD), and the second method is based on the female-years of observation, giving 0.49+/-0.17 births per female per year in this troop. The mean interbirth interval is 21.88+/-6.01 months (mean+/-SD). The mortality of infant born between 2002 and 2005 was 22.4%. The interbirth intervals of females that had lost an infant before the age of 6 months were significantly shorter than that of females whose infants survived for more than 6 months. A female usually gives birth once every 2 years if the previous offspring survives to a weaning age of 5-6 months, or will give birth in the next year if the previous young dies before reaching an age of 6 months. Births were significantly concentrated during March to May of each year. The mean birth date was on April 14, median was April 12; and the standard deviation was 13.98 days. Birth peak occurs 6-7 months after mating peak. From observations on 15 individuals that gave birth for the first time, we concluded that the wild female Golden snub-nosed monkeys in Qinling Mountains start giving birth at an age of 5 or 6 years. We suggest that the seasonal reproductive pattern is an adaptive response to the availability of seasonal food. Our results are consistent with the hypothesis that these reproductive characteristics are a result of adaptation to the seasonality of mountain climate and food resources.     

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although all macaques have a multimale multifemale mating system, the degree of promiscuity shown by the Barbary macaque is considered to be extreme in terms of both mating frequency and number of mating partners. How mating activity is distributed throughout the female menstrual cycle and whether or not copulations are concentrated around the fertile phase as in other members of the genus is, however, not known. To examine this, we collected data on rates of copulation throughout 29 ovarian cycles from 13 free-ranging females of the Gibraltar Barbary macaque population and related them to the time of ovulation and the female fertile phase as determined from fecal hormone analysis. In addition, patterns of male inspection of females and time spent in consortship, both indicators of female attractivity, were also analyzed. The results indicate that both mating behavior and female attractivity vary predictably with ovarian cycle stage. Rates of copulation were found to increase toward the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. Additionally, we show that frequency of inspection of females by males and time spent in consortship were also highest during the fertile phase and that ejaculatory copulations and male pericopulatory behaviors were significantly correlated with levels of female sex hormones. Our findings indicate that the Barbary macaque shows a mating pattern during the cycle similar to that described for other members of the genus. More importantly, however, our study provides clear evidence that despite an extreme degree of promiscuity Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Estrogen-related cues appear to be involved in the process of recognition of female reproductive status by males, but the exact nature of these cues and how male Barbary macaques use them remains to be clarified.     

Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns

The study reports on the use of urinary and fecal hormone measurements for monitoring female reproductive status in captive-housed Hanuman langurs (Presbytis entellus). Matched urine and fecal samples collected throughout 7 complete menstrual cycles of two females, and during part of one pregnancy in a third female were analyzed. Estrone conjugates (E1C) and immunoreactive pregnanediol glucuronide (PdG) in urine and immunoreactive estradiol (E2), progesterone (P4), pregnanediol (Pd) and 20α-hydroxyprogesterone (20αOHP) in feces were measured by enzymeimmunoassay. E1C and PdG in urine were excreted in a cyclic pattern with E1C levels increasing 3- to 4-fold during the follicular phase to reach preovulatory peak values 2 days before a defined rise in PdG concentrations. Cycle lengths ranged between 20 and 34 days comprising a variable follicular phase of 7–21 days and a more consistent luteal phase of 12–14 days. High pressure liquid chromatography (HPLC) analysis of fecal extracts confirmed the presence of all fecal hormones measured, but indicated large amounts of additional immunoreactivity in the three progestin assays. The patterns of excretion of fecal E2 and all three fecal progestins corresponded well with those of steroid metabolites in urine in showing a clear and well defined follicular phase E2 rise followed by a luteal phase progestin increase. Measurement of 20αOHP immunoreactivity revealed the most stable baseline and the highest follicular/luteal phase differential. Levels of all hormones were clearly elevated during pregnancy although urinary E1C and PdG showed a more pronounced increase compared to fecal metabolites. The results indicate that urinary and fecal hormone analysis can be applied to noninvasive monitoring of reproductive status in the Hanuman langur. © 1995 Wiley-Liss, Inc.     

Reproductive events of wild cotton-top tamarins (Saguinus oedipus) in Colombia

Reproductive patterns of wild cotton-top tamarin (Saguinus oedipus) females located in La Reserva Forestal Protectora Serranía de Coraza-Montes de María in Colosó, Colombia, were examined using long-term behavioral observations and fecal steroid analysis. Using an enzyme immunoassay, we analyzed fecal samples for E₁C and PdG. Comparisons of reproductive cycles of a reproductively active female and her daughters were made. An inhibition of ovarian cycles has been observed in daughters living in their families. However, daughters also exhibited normal ovarian cycling that subsequently resulted in pregnancy. Factors influencing the fertility are discussed as they relate to the reproductive strategies of wild cotton-top tamarin females. Am. J. Primatol. 43:329–337, 1997. © 1997 Wiley-Liss, Inc.