Age-dependent changes in fecal 17β-estradiol and progesterone concentrations in female spider monkeys (Ateles geoffroyi)

The objective of this study was to investigate whether sex steroids decreased with age in female black-handed spider monkeys (Ateles geoffroyi). Fecal concentrations of 17β-estradiol and progesterone (five samples/wk) and the number of ovulatory and anovulatory cycles were compared between adult (n = 3) and aged females (n = 2). All animals (regardless of age) had higher 17β-estradiol concentrations during the fertile than the nonfertile phases. However, during the fertile phase, concentrations of this hormone were significantly higher in adult females. Conversely, progesterone concentrations varied normally throughout the menstrual cycle in both adult and aged animals, with no significant difference between age classes. Similarly, there was no significant effect of age on the number of ovulatory and anovulatory cycles. In conclusion, we inferred that the aged female spider monkeys did not reach menopause, instead they remained in a perimenopausal period characterized by changes in fecal concentrations of ovarian steroids and hypothalamus-hypophysis-ovary axis activity, as well as irregular menstrual flows, for prolonged intervals.     

Menopause in female rhesus monkeys

Fifteen female rhesus monkeys (Macaca mulatto), ranging in age from 8 to 34 years, were studied for one year to characterize the endocrine and menstrual changes associated with menopause in this species. Five monkeys were premenopausal; these younger monkeys, ages 8–11 years, menstruated and showed cyclic ovarian activity during the 12–month study period, as evidenced by menses and periodic elevations of serum estradiol (E₂) and luteinizing hormone (LH) concentrations. Four females, ages 24–26 years, were in transition to menopause. Two of these perimenopausal females menstruated and secreted E₂ and LH in a periodic fashion; the other two females showed elevated LH concentrations, consistently low E₂ levels, and no evidence of menstruation. Six females, ages 27–34 years, were clearly postmenopausal; LH concentrations were high, whereas E₂ concentrations were uniformly low. There was a significant inverse correlation between basal E₂ concentrations and age, and a significant positive correlation between age and LH concentrations across all 15 animals. Hormonal changes indicative of ovulation, when they occurred, were generally restricted to the winter and early spring months. Histological analysis of ovaries from four postmenopausal females revealed little or no evidence of active folliculogenesis. These data indicate that menopause in female rhesus monkeys does not occur until the second half of thethird decade of life. © 1995 Wiley-Liss, Inc.     

Seasonal variations of fecal progesterone and 17beta-estradiol in captive female black-handed spider monkeys (Ateles geoffroyi)

A number of studies in free-ranging and captive spider monkeys (Ateles spp.) have shown that this genus is able to reproduce throughout the entire year. Nonetheless, it is still controversial whether births, and therefore conceptions, tend to be more frequent during certain seasons. In the present study, we monitored changes in fecal 17beta-estradiol and progesterone for approximately 1 years in five female black-handed spider monkeys (Ateles geoffroyi) kept in captivity in Mexico City. The objective was to determine whether hormone concentrations and menstrual cycles of summer and autumn accounted for a greater chance of conception than those of winter and spring, consistent with birth patterns previously reported. We collected fecal samples from the five monkeys almost daily for 1 year (March 2004 to February 2005) and used radioimmunoassay of fecal extracts to determine concentrations of 17beta-estradiol and progesterone. Concurrently, menstrual cycle phases were determined by cytological evaluation of vaginal swabs. Periovulatory 17beta-estradiol concentrations were significantly higher in autumn than in winter, spring or summer. Moreover, as evidenced by progesterone peaks, most of the summer-autumn menstrual cycles were ovulatory; in contrast, most of the winter and spring cycles were anovulatory. In conclusion, our data supported the notion that, although not a strictly seasonal reproducer, the black-handed spider monkey is more likely to conceive at the end of the rainy season and throughout autumn.     

Absence of direct effects of prostaglandins on rabbit blastocysts in vitro

A total of 27 monkeys (M. Fascicularis) whose control cycle lengths ranged from 28 to 32 days were used in this study. All the treatments described below started either on day 17 or 18 of the cycle. Six monkeys received daily injections of 20 μg estradiol-17β (E₂) for 5 consecutive days. Although a drop in blood progesterone (P) did occur due to this treatment, no shortening of the luteal phase of the cycle was recorded. Seven monkeys received daily injections of 15 mg PGF_2α (prostaglandin-F_2α) for 4 or 5 days. These monkeys also showed a drop in blood P levels; moreover 5 of these monkeys had vaginal bleeding for 2–3 days starting either on day 19 or 20 of the cycle. This bleeding did not appear to be a normal physiological menstrual flow, since all of the monkeys commenced menstrual flow at the expected time. Four monkeys received daily injections of 10 mg P for 3 days. These monkeys also had normal cycle lengths in spite of the treatment. Finally 9 monkeys received daily injections of 20 μg E₂ for 3 days, and starting on the third day of E₂ treatment these monkeys also received injections of 15 mg PGF_2α for 4 or 5 days. Shortened cycle lengths were recorded in 8/9 monkeys in this group. Six monkeys had 22-day cycles, 2 monkeys had 24-day cycles and the remaining monkey had a cycle length of 26 days. Thus 8/9 monkeys had shortened luteal phases due to sequential treatment of E₂ and PGF_2α. The cycle lengths in all the treatment groups were normal subsequent to treatments. These results provide potentially useful information for further studies in the human as a method of contraception.     

Gustatory Responsiveness to food-associated acids in the spider monkey (Ateles geoffroyi)

The gustatory responsiveness of four adult spider monkeys to five food-associated acids was assessed in two-bottle preference tests of brief duration (3 min). The animals were given the choice between a 30 mM sucrose solution and defined concentrations of citric acid, ascorbic acid, malic acid, acetic acid, or tannic acid dissolved in a 30 mM sucrose solution. With this procedure,Ateles geoffroyi was found to significantly discriminate concentrations as low as 5 mM ascorbic acid, citric acid, and acetic acid, 10 mM malic acid, and 0.1 mM tannic acid from the alternative stimulus. With the latter two substances, the monkeys rejected all suprathreshold concentrations tested, whereas with the former three substances, the animals showed an inverted U-shaped function of preference, i.e. they rejected high concentrations, but significantly preferred low but detectable concentrations of these acidic tastants over the alternative sweet stimulus. The results showed (1) the spider monkey to respond to the same range of acid concentrations as other nonhuman primate species; (2) thatAteles geoffroyi, is able to detect food-associated acids at concentrations well below those present in most fruits; and (3) that unlike most other primate species tested so far, spider monkeys do not generally reject acidic tastants but show a substanceand concentration-dependent change in responsiveness that may range from rejection to preference. The results support the assumptions that spider monkeys may use sourness and/or astringency of food-associated acids as a criterion for food selection, and that the gustatory responsiveness ofAteles geoffroyi to acidic tastants might reflect an evolutionary adaptation to frugivory.     

Female-Directed Aggression in Free-Ranging Ateles geoffroyi

In a study of the reproductive biology and behavior of black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama, 107 instances of female directed male aggression (male attacks) occurred during >1,000 h of observation. Two hypotheses might explain this behavior. First, males may attack to induce defecation/urination by target females, from which they can gain reproductive information. Rates of defecation and urination did not increase subsequent to attacks; however, there was an association between attacks and investigative behaviors such as place sniffing. Alternatively, the attacks might be a form of sexual coercion. My results indicate that female reproductive state, as determined by fecal steroid metabolites (E1C and PdG), had an inconsistent effect on the frequency of attacks received. In addition, when females were in the peri-ovulatory period of the ovarian cycle they did not receive more attacks than at other times. Nor were attacks associated with observed copulations, suggesting that sexual coercion does not sufficiently explain the behavior. Some support is provided for the notion that the attacks allow males to dominate equally-sized females.     

Patterns of estrogen and progesterone receptors in monkey endometrium during the normal menstrual cycle

Total concentrations of estradiol-17β (E₂) and progesterone (P) receptors (R) were measured in the endometrium of rhesus monkeys ($\text{Macaca mulatta}$) during the normal menstrual cycle. The endometrium was collected at abdominal fundal hysterotomy on days 8, 12, 15, 18 and 24 of the menstrual cycle. Visual inspection of the ovaries and measurement of E₂, P, follicle stimulating hormone (FSH) and luteinizing hormone (LH) provided assuredness of normal ovarian function. Exchange procedures were used in order to measure the total concentrations of E₂R and PR in nuclear and cytosol fractions. The pattern of estrogen receptor showed a slight increase in the cytosol and nuclear concentrations at the preovulatory interval. Later, the total E₂R concentration was decreased when P increased during the luteal phase. Cytosol PR synthesis was parallel to the serum E₂ increase during the late follicular phase. Secretion of P by the corpus luteum was accompanied by a rapid nuclear translocation and concomitant decrease in cytoplasmic PR. Thereafter the total PR concentration declined during the second half of the luteal phase. These findings in monkey endometrium are similar to those reported for human endometrium during the normal menstrual cycle and further establish the utility of these surrogate primates in investigations indicative of human endometrial function.     

Social and environmental determinants of reproductive cycles in patas monkeys

The menstrual cycles of a captive group of patas monkeys were followed for 15 months by taking vaginal smears and lavages three times a week. Without an adult male in the group, menstrual cycles still showed the expected qualitative changes previously associated with the onset and with the end of a mating period. The addition of an adult male to the female group, once mating season cycles were evident, did not result in further changes in erythrocytes or sediment levels in vaginal samples or cycle regularity. Menstrual-cycle onsets for related females were significantly more synchronized than onsets for unrelated females. Preliminary observations on adult male patas housed separately from the females indicate that they too undergo seasonal changes in physiology and behavior.     

Some characteristics of the normal menstrual cycle of the bonnet monkey (M. radiata)

Sixty-two menstrual cycles were observed in five bonnet monkeys over a period of 12 months. The menstrual cycles ranged in length from 22 to 35 days, although cycles of from 26 to 29 days were most frequent. Menstrual flow occurred for two to seven days, the flow lasting for three to four days in the majority (82%) of the cycles. Serum estradiol-17β (E₂) and progesterone (P) were measured by radioimmunoassay in two consecutive cycles in each monkey and correlated with changes in the quantity of cervical mucus secretion and spinnbarkeit. The day of the estradiol peak was considered as day 0. The E₂ levels began to rise one to three days before the peak, returning to baseline levels within two days and thereafter remained at low levels. The serum P rose 2 days after the E₂ peak, and maximum level was attained at 10 to 12 days after the E₂ peak. The quantity of cervical mucus increased proportionately with estrogen. However, the quantity remained at maximum levels even after the decline of the serum E₂ level. Similar trends were observed with the spinnbarkeit.     

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157–170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.     

Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (Cercocebus torquatus atys)

Three studies were conducted with female sooty mangabeys to describe the occurrence of perineal swelling during pregnancy and to document the associated patterns of ovarian hormone secretion and sexual behavior. Menstrual cycles and pregnancies were charted in 29 female subjects by recording daily vaginal bleeding and perineal swelling. As in other swelling species, maximum perineal tumescence corresponded with the periovulatory phase of the cycle; however, a second tumescence was recorded during pregnancy, with a peak at 49 days postconception. The swelling patterns were similar with the exception that deturgescence was slower during pregnancy. In a second study, blood samples were obtained weekly from nine females to document the estradiol (E₂) and progesterone (P₄) profiles during pregnancy. Analyses revealed increased E₂ concentrations and low P₄ levels in association with the postconception swelling. A third study compared sexual behavior during ovulatory and post-conception tumescent peaks. Behavioral data revealed that, although there was no overall difference in male mount rate to females during the ovulatory and postconception maximum swelling period, when only the alpha male was considered, significantly fewer mounts were directed to females exhibiting a post-conception versus an ovulatory maximum tumescence.     

Serum 17β-estradiol and progesterone associated with mating behavior during early pregnancy in female rhesus monkeys

The phenomenon of postconception mating behavior was examined in a social group of rhesus monkeys living in an outdoor compound. Periodic blood samples and daily vaginal swabs were obtained from nine females beginning several weeks prior to conception and continuing through 6 weeks of pregnancy to permit an assessment of ovarian hormonal events associated with mating during early pregnancy. Each of the females showed a discrete period of copulatory activity during the periovulatory period which ceased within several days after the 17β-estradiol (E₂) ovulatory peak. In agreement with earlier reports, only a percentage of subjects (44%) exhibited a period of postconception mating, with copulatory activity beginning 19.8 (± 1.9) days following the E₂ peak and continuing for 9.5 (± 1.3 days). Implantation bleeding was detected in all of the subjects with the onset 19.5 (± 0.68) days after the E₂ peak. The interval between the E₂ peak and the onset of implantation bleeding was similar for all females. However, the duration of implantation bleeding was significantly shorter in females who exhibited postconception mating. The females who displayed postconception copulatory activity had significantly lower mean serum progesterone concentrations (2.33 ± 0.24 ng/ml vs. 3.64 ± 0.37 ng/ml) during the period associated with implantation bleeding and copulatory behavior. Although both groups had elevated concentrations of serum E₂ during this period, levels in the females who displayed postconception mating were significantly lower (173.8 ± 19.2 pg/ml vs 223.9 ± 28.8 pg/ml). These data demonstrate that the occurrence of postconception mating behavior in this environment is associated with a distinct pattern of ovarian hormonal events, and analysis suggests that differences in steroid concentrations probably account for the observed differences in implantation bleeding and copulatory behavior during pregnancy.     

Induction of atresia of the dominant follicle in rhesus monkeys (Macaca mulatta) by the local application of estradiol-17β

Estradiol-17β (E₂), administered systemically to rhesus monkeys during the follicular phase of the menstrual cycle, induces atretic changes in the microenvironment of the dominant follicle (DF), which results in its demise. It has been proposed that this effect of E₂ represents a direct action at the ovarian level. The present study was designed to test this hypothesis, using local treatment with E₂. After identification of the DF during laparoscopy on day 6 of the cycle, female monkeys were laparotomized and their ovaries exposed. Either corn oil (20 μl, controls) or E2 (100 μg ) in oil vehicle (experimentals) was injected into the ovary near the DF. In control animals, preovulatory release of gonadotropins and ovulation were normal in five of six animals, with cycle and luteal phase lengths of 27.8 ± 2.2 days and 14.6 ± 2.5 days, respectively (x? ± S.D.). Conversely, in only one of six animals in the experimental group did ovulation occur at the expected time (P < 0.05). In the other five treated animals, E₂ induced atresia of the DF and significantly extended cycles (35.4 ± 5.4 days) without affecting luteal phase lengths (12.0 ± 1.4 days). Concentrations of estrogen in peripheral sera of some animals were increased transiently at 6 h after injection of E₂ but returned to normal by 12 h; this duration of estrogen exposure is far less than the 24 h required to induce atresia of the DF in previous studies. At 6 h after injection of E₂, there was a statistical difference between controls and experimentals in concentrations of circulating estrogen; however, these changes were apparently not enough to alter pituitary secretion of follicle-stimulating hormone or luteinizing hormone. These data support the hypothesis that E₂ can induce atresia of the DF in rhesus monkeys by acting locally at the ovary.     

Feeding ecology of spider monkeys (Ateles geoffroyi) at Tikal,Guatemala

Field study in tropical dry forest in Tikal National Park, Guatemala, revealed that spider monkeys (Ateles geoffroyi) devoted about 57% of feeding time to fruit (pulp), 20% to the unripe seeds of a single tree species, and the remainder largely to leaves and buds. Fruit, seeds, flowers and leaves ofBrosimum alicastrum (Moraceae) accounted for 56% of the diet, and there was very little predation on invertebrates. A severe drought occurred during 1975, the first year of the study, and a comparison between July of that year with July, 1978 shows that in the drought year there was heavier than normal reliance on fruit of the genusFicus (46% versus 14%) and depressed consumption ofBrosimum (11% vs. 54%). Dietary species diversity (Shannon's measureH) and evenness (Hill'sE) were markedly higher during the drought July than the normal July.     

Gustatory thresholds for food-associated sugars in the spider monkey (Ateles geoffroyi)

The purpose of this study was to determine gustatory thresholds for five different food-associated sugars in Ateles geoffroyi. Using a two-bottle test, three adult spider monkeys were found to significantly prefer concentrations as low as 3 mM sucrose, 15 mM fructose, 20 mM glucose, and 10 mM lactose over tap water. Maltose was significantly discriminated down to 20 mM with individual animals showing either a preference or an aversion, or an inverted U-shaped function of preference toward higher concentrations of this carbohydrate. The results showed the spider monkey to respond to lower sugar concentrations compared to other nonhuman primates tested so far and thus support the assumptions that Ateles geoffroyi may use sweetness as a criterion for food selection, and that the remarkably high sweet-taste sensitivity of this frugivorous species might be correlated with its dietary specialization. © 1996 Wiley-Liss, Inc.     

Phylogenetic Relationships of Spider Monkeys (Ateles) Based on Mitochondrial DNA Variation

Our goal was to determine phylogenetic relationships among geographically and taxonomically distinct haplotypes of spider monkeys (Ateles) based on DNA sequence variation for the mitochondrial DNA control region and cytochrome c oxidase subunit II gene. We obtained samples from most previously recognized subspecies of Ateles, ranging from Central America throughout the Amazon Basin, to determine phylogenetic relationships among racially recognized groups. Comparison of DNA sequences using both parsimony analysis and genetic distance analysis produced phylogenetic relationships that were very similar for each genetic region. We analyzed the phylograms produced, along with associated bootstrap support, confidence probabilities, and genetic distances between taxonomic groups, to identify four monophyletic species of Ateles: Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; A. belzebuth in the southern Amazon Basin; A. hybridus, located primarily along the Magdalena River valley of Colombia; and A. geoffroyi, which includes two former species: A. geoffroyi and A. fusciceps. This arrangement is contradictory to long-held taxonomies of Ateles based on pelage variation and is similar to a recent analysis based on craniodental variation. Results of this investigation suggest patterns of gene flow, evolutionary relationships, and speciation patterns that are more plausible than previous pelage-based taxonomies, which required seemingly impossible patterns of gene flow. Conservation efforts aimed at protecting Ateles, one of the Neotropics most endangered genera, will also benefit from the findings presented in this paper.     

Primates hunting by Guaymi amerindians in Costa Rica

This paper discuss the socioeconomical and cultural motivations for hunting primates between the Guaymi amerindian native population in Costa Rica, and their ecological implications. Meat consume rate between Guaymi population is very low, less than one time each week. Only 51% of the population use primates like food ocasionally, andAteles geoffroyi shows to be the preferred meat source. Instead of that fight against crop raiders becomes here an important reason to shot primates. All the inquiered claim thatCebus capuchinus is the most destructive species. Other traditional uses of the primates found between Guaymis is the supposed medicinal value of some species, and its condition of preferred pets. Howler monkeys (Alouatta palliata) are hunted to get their fat that is considered a usefull medicine. The species found more frequently like pets areAteles geoffroyi andCebus capuchinus.     

Atretogenic action of estrogen in rhesus monkeys: Effects of repeated treatment

The effects of 17β-estradiol (E₂), administered in Silastic capsules for 24 hours at intervals of 10 or 14 days, on follicular development and menstrual cycle characteristics were studied in 13 rhesus monkeys. In seven monkeys receiving E₂ at l0-day intervals for 50 treatment periods, new follicles frequently developed between treatments but usually regressed. In seven instances, the follicles persisted longer than expected but were steroidogenically suppressed and regressed spontaneously. Ovulation occurred in only two instances. In six monkeys receiving E₂ at 14-day intervals, new follicles developed regularly, with seven ovulations occurring in 37 treatment periods. A persistent anovulatory follicle was noted in only one instance. Menstruation occurred with equal frequency, and the interval from treatment to onset of menstruation was not significantly different regardless of treatment or the occurrence of ovulation; the intervals between menstruation approximated those of normal menstrual cycles. In general, following termination of treatment, menstrual cycles returned to normal quickly. These data indicate that E₂ administered intermittently at 10-day intervals effectively suppresses ovulation, and they provide new insight into the actions of E₂ on folliculogenesis in primates.     

The effect of female proximity and social interaction on the menstrual cycle of crab-eating monkeys (Macaca fascicularis)

Twelve adult female crab-eating monkeys (Macaca fascicularis) were placed in six pairs of adjacent cages, allowing physical contact between members of these experimental pairs. Twelve additional females remained singly caged (no physical contact allowed) and served as six control “pairs.” In both experimental and control pairs, one member had a history of regular menstrual cycles, whereas the other tended to have cycles that were unusually long and/or irregular. Over a six-month period, menses and amount of vaginal secretion were recorded daily for all subjects, and the behavior of experimental pairs was sampled three times per week. During the course of the study, the irregular experimental subjects began to exhibit menstrual cycles of near normal length although there was no apparent trend to synchronize cycles. Irregular controls continued to show cycles that were abnormally long. Vaginal secretions tended to increase in all regularly cycling animals during days 9–15 (peak day 11) or reverse days 21–16 of the cycle, consistent with the estimated time of ovulation. Analysis of behavior indicated that irregularly cycling subjects inspected the genitalia of their regularly cycling cagemates at a significantly higher frequency than the converse (F=12.61,p<.005), particularly during the follicular phase (F=3.39,p<.07). These results suggest that close physical contact may serve to transmit chemical and/or hormonal cues that can normalize the menstrual cycle of crab-eating monkeys.