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.     

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.     

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis)

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.     

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.     

Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi)

I report three cases of coalitionary aggression by adult male black-handed spider monkeys (Ateles geoffroyi) against subadult males within their community on Barro Colorado Island (BCI), Panama. Two of these cases were followed by the disappearance and presumed death of the victim. Similar behavior was recently reported by Valero et al. [in press], who suggested that this behavior may be the result of intense male reproductive competition. Like the single instance they reported, the cases I report all occurred when the operational sex ratio was approximately 1:1, which suggests that intense competition among males for access to reproductively viable females may be a contributing factor. Additionally the very low density of spider monkeys on BCI may play a significant role in the occurrence of this lethal aggression. Large numbers of adult males are not necessary to protect a territorial boundary against neighboring groups, and additional males may act merely as mating competition.     

Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus)

In many primate species, conspicuous behavioral and/or morphological changes are indicators of the fertile phase of the female cycle. However, several primate species, such as the white-faced capuchin, lack these cues. This is referred to as "concealed ovulation," and is argued to be a reproductive strategy that confuses paternity and lowers the risk of infanticide. We studied 10 adult female white-faced capuchins in Santa Rosa National Park, Costa Rica, from January to June 2002. We determined their ovarian cycling patterns by analyzing fecal ovarian hormones, and compared simultaneously collected behavioral data to determine which, if any, cues females use to signal their fertile phases. We found that four females cycled during the study period but ceased to cycle without becoming pregnant. We considered several explanations for the lack of conception during our study, including reproductive seasonality. We found that female C. capucinus showed only small increases in rates of affiliative/proceptive behaviors directed toward adult males during their periovulatory phases. The best indicator of cycle phase was a significant increase in male affiliative behaviors (e.g., following and grooming bouts) and sexual behaviors (e.g., copulations and courtship displays) directed toward females during the periovulatory phase compared to the nonovulatory phase. Our finding that females exhibit little proceptive behavior, but that copulations and male courtship are nonetheless concentrated in periovulatory phases suggests that even though females do not provide behavioral and morphological cues to ovulation, males are still able to detect it. Infanticide occurs with some frequency in these monkeys, and there is evidence for postconceptive mating as a female strategy to lower risk of infanticide via paternity confusion. However, despite this occurrence of nonconceptive mating and the absence of female cues to ovulation, truly concealed ovulation does not appear to be characteristic of this study population of white-faced capuchins.     

Does Estradiol Modulate Sexual Solicitations in Female Rhinopithecus roxellana?

Studies of the relationship between sexual behavior and reproductive endocrinology in females offer critical insight into sexual selection, mate choice, and female reproductive strategies in primates. We examine the relationship between sexual solicitations and urinary estradiol in female Sichuan golden monkeys (Rhinopithecus roxellana) living under semiwild conditions at the Shanghai Wild Animal Park, China. We collected data on the frequency of sexual solicitations and urinary samples on 4 adult females during 2 mating seasons. We determined urinary estradiol levels via radioimmunoassay. Our results indicate that during the ovarian cycle, solicitation focused on the periovulatory period around the estradiol peak. The frequency of female solicitations rose to a peak after the peak of estradiol level, suggesting that ovarian steroids modulate sexual behavior during the fertile phase of the ovarian cycle. We also found that females frequently solicited matings during pregnancy, most of which the α male accepted and that resulted in copulations. During pregnancy, however, there was no obvious relationship between sexual solicitation and urinary estradiol. We conclude that in Rhinopithecus roxallana, sexual behavior and estradiol production do not strictly correlate during different parts of the reproductive cycle. We discuss additional relationships between social interactions, dominance, sexual behavior, and endocrine function.     

Female-directed Male Aggression in Wild <Emphasis Type="Italic">Ateles geoffroyi yucatanensis</Emphasis>

Male spider monkeys direct the majority of their aggression toward adult females, and the aggressive interactions may be a form of sexual coercion. We investigated female-directed male aggression in 2 wild communities of spider monkeys (Ateles geoffroyi yucatanensis) from the Otoch Ma’ax Yetel Kooh Reserve in Yucatan, Mexico to evaluate the sexual coercion hypothesis. The aggression occurred in 2 distinct forms: physical aggression and prolonged noncontact chases. The latter appeared highly ritualized in nature and accounted for >80% of all female-directed male aggression. Rates of prolonged chases, but not physical aggression, peaked when the female target was likely cycling and were associated with male place-sniffing of the substrate previously occupied by the female target. Prolonged chases were also associated with proceptive behavior directed from the female target toward her male attacker after the chase had ceased. Our data therefore suggest that prolonged chases are sexually motivated. Prolonged chases did not result in immediate copulation, but sometimes the female victim left the subgroup to travel alone with her male aggressor, and thus prolonged chases may be a form of male intimidation to coerce females into a mating consortship. However, as prolonged chases appeared highly ritualized, the chases may also be a form of male sexual display. Further investigation of the costs incurred by female recipients of prolonged chases is therefore required before one can interpret the behavior as sexual coercion.     

Mating behavior and endocrine profiles of wild black and white Colobus monkeys (Colobus guereza): toward an understanding of their life history and mating system

Black and white colobus monkeys (Colobus guereza, "guerezas") show no external signs of estrus, and little is known about their mating behavior or reproductive endocrinology. To learn more about the life history characteristics and mating system of guerezas, we documented the mating behavior and ovarian hormone profiles of 10 cycling, lactating, and pregnant females in a wild population. We studied six groups of guerezas in Kibale National Park, Uganda, and collected ad libitum data on their mating behavior. We collected urine samples every 1.9+/-0.2 days from potentially fertile females and quantified conjugated urinary estrogen (E1S) and progesterone (PdG) metabolites using enzyme immunoassay (EIA). Females solicited 50.5% of copulations, and most copulations occurred during the interval starting 5 days before presumptive ovulation and ending 2-3 days later, with the highest copulatory levels occurring close to ovulation. We show that the median ovarian cycle length is 24 days, the median gestation length is approximately 158 days, the length of lactational amenorrhea is at least 7-8 months, and the median interbirth interval for females with surviving infants is approximately 22 months. We also document overlap between females' receptive periods in one-male, two- to three-female groups, which may mean that male transfer into such groups is potentially profitable.     

Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi)

I report ad libitum data on 18 copulations involving free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama. All copulations were performed in a dorsoventral position, as is typically reported for this genus. Intromission often appeared difficult to achieve, possibly as a result of the large size of the glans penis in these animals. The average length from intromission to termination of thrusting exceeded 17 min, followed by an average period of almost 2 min before separation occurred, which suggests the possibility of a copulatory lock. Offspring of the female participant were almost always in close proximity to or in contact with the pair, and harassment by the offspring was observed only during the final stages of the copulation. All but one copulatory event occurred in complete seclusion from other adult males, and sexual behavior was not limited to any one adult male in the group.     

The menstrual cycle of the spider monkey (Ateles geoffroyi)

The ovarian cycles of four adult female spider monkeys (Ateles geoffroyi) were followed daily throughout 30 days by means of vaginal swabs and blood samplings. Cytological analyses of the vaginal swabs and radioimmunoassay determination of the daily levels of estradiol-17β (E₂) and progesterone (P₄) were done in order to classify the kind of ovarian cycle of this species. Our results show that Ateles geoffroyi females display menstrual cycles of about 24 days on average. By comparison with the well-known menstrual cycles of women, apes, and Old World monkeys, the four distinctive cytological phases (bleeding, follicular, periovulatory, and luteal) could be recognized; mid-cycle E₂ peaks followed by mid-luteal increases of the same hormone were present in all four females. P₄ levels were higher after the E₂ peak, although both hormones were present throughout the cycles. Also, age-dependent features, hormone profiles, and changes in menstrual phases lengths were detected. Am. J. Primatol. 44:183–195, 1998. © 1998 Wiley-Liss, Inc.     

Extended postpregnancy estrous cycles in fernale lion-tailed macaques

Past studies of female primate reproduction have focused on regularly cycling females, and thus the reproductive characteristics of females in other reproductive states (e.g., pregnant, or lactating) have rarely been investigated. In this study, data were collected on estrous swellings and sexual and proceptive behavior in six female lion-tailed macaques during recovery from lactational amenorrhea for the first three to five postpregnancy cycles. For these females, the length of the first lactational recovery swelling cycle averaged 81 days, nearly three times the length of cycles exhibited by nonparturient, isosexually housed females Actual swelling durations were also nearly three times the length of those seen in nonlactating females, and occupied a larger proportion of the cycle For most females, cycle duration and sexual and proceptive behavior declined progressively over successive cycles. The alpha female in each group accounted for the majority of copulations in the first three cycles, and this effect was pronounced in the first cycle. Extended postpregnancy cycles in this species may be related to female reproductive competition and /or a tactic to attract extra-group males. © 1993 Wiley-Liss, Inc.     

Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe Giraffa camelopardalis

Female distribution exerts a major impact on male mating tactics. Giraffe cows have a reproductive cycle, and a social system, that should favor a male roaming reproductive tactic. We conducted a 2-year study of female Rothschild's giraffe (G. c. rothschildi) reproductive endocrinology in order to characterize attributes of the reproductive cycle and investigate how female endocrine and behavioral cues influence mating activity. We used non-invasive fecal steroid methods to determine reproductive state among females residing in a herd in a large outdoor enclosure. We found that females had an estrous cycle of 14.7 days and that they regularly had multiple ovarian cycles prior to conception. Adult males were more likely to associate with, and sexually investigate, females when they were cycling than when they were either pregnant or acyclic. During the estrous cycle, male-female proximity and sociosexual behavior were more pronounced during the probable fertile phase than the rest of the cycle. Sexual activity between giraffe coincided with the periovulatory period, with male interest in females peaking during the fertile window in the absence of proceptive behavior by females. We conclude that males detect reliable cues revealing female reproductive status and partition their reproductive effort in response to such cues. We propose that male giraffe adopt a roaming reproductive strategy with their large size, enabling them to search for and mate guard fertile females while minimizing metabolic costs.     

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.     

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.     

Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles geoffroyi) in Panama

Members of the population of black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama, use the leaves of three Rutaceae species in a behavior that resembles fur rubbing in the white faced capuchin (Cebus capucinus). This behavior has not been reported from other sites where Ateles has been studied. During more than 1,200 hours of observation, 30 episodes of this behavior were recorded ad libitum. Adult males engage in this behavior more than adult females. Season did not impact the frequency of the behavior. The behavior described here differs in many respects from that reported for Cebus capucinus, and does not fit the hypotheses that the behavior functions in repelling insects or other antiseptic purposes. It is proposed that fur rubbing in this group of spider monkeys is a modification of a behavior previously recorded in Ateles and may function in scent marking.     

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.     

Tool use in wild spider monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)

Tool use has been observed in a variety of primate species, including both New and Old World monkeys. However, such reports mainly address the most prodigious tool users and frequently limit discussions of tool-using behavior to a foraging framework. Here, we present observations of novel and spontaneous tool use in wild black-handed spider monkeys (Ateles geoffroyi), where female spider monkeys used detached sticks in a self-directed manner. We introduce factors to explain Ateles tool-using abilities and limitations, and encourage the synthesis of relevant research in order to gain insight into the cognitive abilities of spider monkeys and the evolution of tool-using behaviors in primates.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.