Sexual behavior in brown capuchins ( Cebus apella )

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Sexual behavior in brown capuchins (Cebus apella)

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Female mate choice and male–male competition in Tonkean macaques: Who decides?

The theory of sexual selection predicts that females should be discriminatory in the choice of sexual partners. Females can express their choice in two ways. In direct mate choice, they show preferences for certain partners. In indirect mate choice, they select partners by displaying sexually attractive traits, thus eliciting contest competition between males. We focused on a primate species in which females advertise the timing of their ovulation and studied the balance between these two choice strategies. We tested predictions related to three hypotheses about direct and indirect female choice, namely the best‐male, graded‐signal and weak‐selectivity hypotheses. We investigated the sexual and agonistic interactions occurring during oestrous periods in five captive groups of Tonkean macaques (Macaca tonkeana). The results showed that dominant males used mate guarding to monopolise sexual access to parous females that were in the fertile stage of their reproductive cycle, while lower‐ranking males monitored only nulliparous females. The distribution of sexual presentations indicated that females accepted different types of partners, supporting the weak‐selectivity hypothesis regarding direct mate choice. The analysis of behavioural sequences revealed that mate‐guarding males used mild coercive behaviours to prevent females from mating with other males at conception time. The distribution of mounts showed that females mainly mated with dominant males, which leads us to argue that the best‐male hypothesis provides the most parsimonious explanation regarding indirect mate choice in Tonkean macaques. At the individual level, it may be concluded that male competitive strategies prevented females from exercising direct mate choice. At the evolutionary level, however, female sexual advertising and thus indirect choice promoted competition between males. The outcome is that indirect mate choice appears more important than direct mate choice in female Tonkean macaques.     

Females Pay Attention to Female Secondary Sexual Color: An Experimental Study in <Emphasis Type="Italic">Macaca mulatta</Emphasis>

Researchers have long considered the color of female sexual skin to play a role in attracting or inciting competition among males, or both; however, females may also use color in intrasexual communication. To assess this possibility, we examined whether variation in same-sex sexual skin color is salient to female rhesus macaques (Macaca mulatta). We exposed adult females to computerized images of conspecific female faces and hindquarters manipulated for color (red vs. non-red), within the natural range of color variation. Females visually attended more to both reddened faces and hindquarters over the non-red counterparts. We conclude that female color might be biologically meaningful to other females.     

Evidence for sexually selected infanticide in captiveCercopithecus mitis,Cercocebus torquatus,andMandrillus leucophaeus

Adult resident males of one-male-multi-female primate groups housed at the Hannover Zoo exhibited aggression, when confronted with nonadult individuals, which were fathered by other males: (1) a new adult resident male in a group of blue monkeys killed a 5.8-month-old female infant: (2) a new adult resident male in a group of white collared mangabeys injured a 24.0-month-old female and an 18.9-month-old male severely; they would have died without veterinary care; and (3) the resident male of a group of drills threatened an 1.8-month-old foreign female infant seriously; efforts to introduce the infant were discontinued. Pathological explanations are unlikely because the adult males showed no aggression towards own nonadult offspring under the same captive conditions. By and large, the events support the theory that infanticide is the result of sexual selection among males.     

Female Copulation Calls in Guinea Baboons: Evidence for Postcopulatory Female Choice?

We tested the hypothesis that primate female copulation calls are a form of postcopulatory female choice. We collected data on female sexual swellings, sexual and agonistic behavior, copulation calls and postcopulatory behavioral interactions in a multimale-multifemale captive group of Guinea baboons over a 3-mo period. Males copulated with only a few females, and females copulated with only 1 or 2 different males in the group, suggesting a harem-like mating system similar to that of hamadryas and gelada baboons. Female copulations were most likely to occur at peak sexual swellings and male copulatory success was accounted for by dominance rank and age. Variation in female tendencies to call after copulation is best explained by the copulatory success of the male with which each female copulated the most and by the number of copulating partners. The findings are consistent with predictions that calls are likely to be associated with copulation with preferred males and the risk of sperm competition. The prediction that copulation calls increased the probability of postcopulatory mate guarding is also supported. Taken together, the findings suggest that female copulation calls may play an important role in postcopulatory sexual selection and in particular in the expression of postcopulatory female choice in primate species in which females have little opportunity to choose their mates or female mate choice is costly or both.     

Effects of dominance and female presence on secondary sexual characteristics in male tufted capuchin monkeys (Sapajus apella)

Alpha status may lead to physiological changes that enhance secondary sexual characteristics, which may serve as competitive signals to conspecific males, sexual signals to females, or possibly a combination of both. Here, we report measurements of secondary sexual characteristics in captive dominant and subordinate male tufted capuchin monkeys (Sapajus apella) with varying access to females. An adult male (who had previously been subordinate while housed with other males) was paired with an adult female. This male–female pair was introduced into a room that housed three other male–male pairs with stable hierarchy arrangements. We analyzed weight, body measurements, facial photographs, and hair cortisol before, during, and after introducing a female into the room. While there were no differences in weight or measurements between alphas and subordinates without physical access to the female prior to or during the female''s presence, we found that direct access to the female resulted in dramatic changes in facial appearance, body size, and testicular volume in the male who was paired with her. Overall, we found little evidence to suggest that alpha males advertise their status within all‐male groups via sexual secondary characteristics. However, direct physical access to females appears to trigger the development of such characteristics in alpha males. It remains of continued interest to identify the endocrine mechanisms responsible for the development, and possible loss, of secondary sexual characteristics.     

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.     

Scent-marking behaviour by male prairie voles,Microtus ochrogaster,in response to the scent of opposite- and same-sex conspecifics

We conducted an experiment using the prairie vole (Microtus ochrogaster) to test predictions associated with the proposed functions of scent marking as a sexual attractant, in reproductive competition, and as a self-advertisement. We allowed an oestrous female, an anoestrous female, and an adult male to scent mark three portions of a clean substrate and then exposed a second male to this substrate for secondary marking. We did not support a sexual attraction hypothesis in that males did not place more scent marks in response to oestrous than anoestrous females. Similarly, we did not support a reproductive competition hypothesis in that males did not place more scent marks in response to marks of males than to those of females or bare substrate. Males did not overmark the scent of males or females and thus we did not support a scent-masking or scent-blending hypothesis. In that males deposited scent similarly in response to males, females, and on bare substrate, our results suggest that the frequency and placement of scent marks by males function primarily to advertise individual identity in an area.     

Female relationships in bonobos(Pan paniscus)

The popular belief that women are not naturally able to bond with each other is often supported by theoretical and empirical evidence that unrelated females do not bond in nonhuman primate species. Bonobos (rare and endangered African apes, also known as pygmy chimpanzees) are (with their congener, chimpanzees) the closest living relatives of humans and appear to be an exception to this characterization. Data collected on individuals representing half of the world’s captive population reveal that bonobo females are remarkably skillful in establishing and maintaining strong affiliative bonds with each other despite being unrelated. Moreover, they control access to highly desirable food, share it with each other more often than with males, engage in same-sex sexual interactions in order to reduce tension, and form alliances in which they cooperatively attack males and inflict injuries. Their power does not stem from a size equality with or advantage over males (in fact, females average 82.5% of male size), but rather from cooperation and coalition formation. The immediate advantage to female alliances is increased control over food, the main resource on which their reproductive success depends, as well as a reduction in other costs typically associated with a female-biased dispersal system, such as male agonism in the contexts of feeding competition and sexual coercion. The ultimate advantage of friendly relationships among females is an earlier age at first reproduction, which results in a large increase in lifetime reproductive success. Analysis of this bonding phenomenon sheds light on when, where, and how we should expect unrelated human females to bond with one another by demonstrating that bonding is not dependent on access to one’s relatives but rather on an environmental situation in which female aggregation is possible, coupled with an incentive for cooperation.     

Courtship herding in the fiddler crab <Emphasis Type="Italic">Uca elegans</Emphasis>

Male and female animals are not always complicit during reproduction, giving rise to coercion. One example of a system that is assumed to involve sexual coercion is the mate herding behaviour of fiddler crabs: males push females towards the home burrow with the goal of forcing copulation at the burrow entrance. We recorded and analysed in detail the courtship behaviour of a North Australian species of fiddler crab Uca elegans. Courtship was composed of four main phases: broadcast waving, outward run, herding and at burrow display. During interactions males produced claw-waving displays which were directed posteriorly towards the female and which varied in timing and structure depending on the courtship phase. We suggest that courtship herding in U. elegans is driven primarily by mate choice for the following reasons, (1) females can evade herding, (2) no other reproductive strategies were observed, (3) males broadcast their presence and accompany courtship with conspicuous claw waves, and (4) the behaviour ends with the female leading the male into the home burrow. As an alternative function for herding in U. elegans we suggest that the behaviour represents a form of courtship guiding, in which males direct complicit females to the correct home burrow.     

Social Behavior,Reproductive Strategies,and Population Genetic Structure of <Emphasis Type="Italic">Lagothrix poeppigii</Emphasis>

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon. Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.     

Male-male competition and mating success in the orb-web spider,Nephila clavata,with reference to temporal factors

Seasonal occurrence patterns of adults of both sexes, intensity of male-male interactions, and mating success in the spider,Nephila clavata, were examined in the field. Adult males began to attend female webs about 2 weeks before female maturation. Large adult males were abundant in the early breeding season, but small males increased later in the season. From the distribution of males among female webs and size relationship of males within a web, male-male interactions seemed to be more intense when most females were still subadult. This was verified by a field experiment in which males were artificially introduced to female webs that were attended by other males. It was found that the probability of introduced males remaining on subadult female webs was lower than that on adult webs. As mating occurred mostly in the period shortly after the female final molt and first male sperm precedence was known in all spiders reported so far, intense male-male competition on subadult female webs seemed to be reasonable. Male longevity had an important influence on the mating success of males with just-molted females. Mating success was also affected by the relative body size of males present in a given period. Since larger males occupied the position closest to females within a web and stayed there longer, relative body size appeared to influence mating success through male-male competition. Female body size at maturation declined with time; hence, males that attained sexual maturity earlier had the advantage of mating with larger and more fecund females. Therefore, early maturation as well as larger size seem to be two important trairs influencing the reproductive success of males.     

Mating system in mouse lemurs: theories and facts, using analysis of paternity

Among nocturnal Malagasy prosimians, the grey mouse lemur (Microcebus murinus) is considered a solitary species which has a promiscuous mating system. Indirect indicators, such as the lack of sexual dimorphism, the overlapping of male and female home ranges with each other, the synchronism of seasonal oestrus and the high relative testes size of males, support the presence of sperm competition. In captivity, an intense sexual precopulatory competition develops among males, leading to the emergence of a dominant male who fathers the majority of the litters. Although multiple mating did occur, the dominant male achieved the majority of the matings on the first day of oestrus. A 'mate-guarding' behaviour, exhibited by the dominant male, was observed in 11 groups out of 15, on only the first day of the vaginal opening and was significantly more often directed towards younger females. Females also played an important role in sexual competition among males, since their presence enhances the aggressive interactions between males. Difference in aggressive behaviours of females, in response to male sexual solicitations, suggests female mate choice. Compared with data from wild animals, it may be hypothesised that alternative mating strategies can be used by male grey mouse lemurs to enhance their reproductive success, depending on the availability and distribution of receptive females.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

Female sexual behavior in the absence of male-male competition in captive Japanese macaques (Macaca fuscata)

A captive group of Japanese macaques (Macaca fuscata). consisting of one adult male and three adult females, was observed for 88 hr during the 1988 mating season. We focused on the group's sexual activities because understanding how social dynamics affect reproductive behavior may enhance our ability to establish self-sustaining captive populations. The adult male exhibited distinct preferences in copulation partners, although all females were receptive and cycled during the study period. The dominant female participated in the most copulations and successfully harassed and disrupted copulations between the male and the other females. The alpha female, therefore, actively constrained the formation of mating pairs. Further, the male did not consort with his year-round female grooming partner. This female, the least dominant member of the group, engaged in the most autosexual and homosexual behavior. Birth season data show that only the dominant female bore offspring. This study emphasizes the influence of social dynamics on a group's reproductive potential and suggests an alternative means by which females can influence consort formation.     

The Starling Mating System as an Outcome of the Sexual Conflict

Many bird species demonstrate a variable mating system, with some males being monogamously mated and other males able to attract more than one mate. This variation in avian mating systems is often explained in terms of potential costs of sharing breeding partners and compensation for such costs. However, whenever there is a difference in the optimal mating system for males and females, a sexual conflict over the number of partners is expected. This paper contains a verbal model of how a conflict between male and female European starlings (Sturnus vulgaris),resulting from the fitness consequences of different mating systems for males and females differing over time, determines the mating system. We demonstrate that males and females have contrasting fitness interests regarding mating system, such that males gain from attracting additional mates whereas already mated females pay a cost in terms of reduced reproductive success if males are successful in attracting more mates. We demonstrate how this can be traced to the rules by which males allocate non-sharable care between different broods. Furthermore, we demonstrate that there exist male and female conflict behaviours with the potential to affect the mating system. For example, aggression from already mated females towards prospecting females can limit male mating success and males can circumvent this by spacing the nest-sites they defend. The realised mating system will emerge as a consequence of both the fitness value of the different mating systems for males and females, and the costs for males and females of intersexual competition. We discuss how this model can be developed and critically evaluated in the future.     

Seasonal Changes of Vocal Rates and Their Relation to Territorial Status in Male Galápagos Sea Lions (Zalophus wollebaeki)

Male vocal displays play an important role in sexual selection through both male–male competition and female choice. While this is supported by numerous studies in birds, much less attention has been paid to the role of such displays in mammals. We investigated the function of vocal displays in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki). In our study population a large proportion of mature males are unable to establish a territory, providing the opportunity to compare the vocal behaviour between territorial and non‐territorial males. We examined how seasonal patterns of vocalizations differed between territorial and non‐territorial males and how the number of females present in a territory influenced behaviour of territorial males. We found that territorial males vocalized at higher rates than non‐territorial males, and territorial males vocalized more at the onset than towards the end of territory tenure. During the onset of territory‐tenure vocalizations of territorial males were directed more often towards other males than females. Furthermore, we found that vocalizations of territorial males were not only given in male–male interactions, but were also actively directed towards females. Territorial males vocalized at higher rates when more females were present in their territory. Our results suggest that vocalizations are important in male–male interactions, are relevant in territorial disputes and are used as a proxy for females to assess a male’s quality.     

Interactions of social,spatial and hormonal factors on the behavior of rhesus monkeys (Macaca mulatta)

In a three year study, the interactions of social, spatial and hormonal variables on the behavior of rhesus monkeys were investigated. Observations were made on (1) an oppositelysexed pair alone in a cage; (2) the pair alone in a large room; and (3) the pair together with three ovariectomized females in the same large room. Each of four males was tested with the same group of four ovariectomized females (16 pairs, 480 1-hr tests). Each female served in turn as the focal female, namely, the hormone-treated one, and received first estradiol benzoate (EB) alone and then in combination with progesterone (P). The presence of three other females (the social variable) had a marked effect on all aspects of the behavior of the focal pair, and reduced the male's ejaculations as well as other sexual and affiliative interactions with the focal female. This was due to an inhibitory influence exerted by the dominant female on the interactions of subordinate females with the male. Comparing data from two groups of females showed that female dominance rank, and not male sexual preference, was the critical factor, and that mate competition between female rhesus monkeys was operating. Decreasing the space available for the interactions of the pair appeared to imitate a bonding effect in the male, increasing male grooming and tending to increase male sexual activity. In the group setting, treating the female with EB increased sexual activity, and additional progesterone decreased it in all three test settings. The effects of progesterone were most clearly apparent when the pair was tested alone in a large area.     

Multiple paternity in a natural population of a salamander with long-term sperm storage

Sperm competition appears to be an important aspect of any mating system in which individual female organisms mate with multiple males and store sperm. Post-copulatory sexual selection may be particularly important in species that store sperm throughout long breeding seasons, because the lengthy storage period may permit extensive interactions among rival sperm. Few studies have addressed the potential for sperm competition in species exhibiting prolonged sperm storage. We used microsatellite markers to examine offspring paternity in field-collected clutches of the Ocoee salamander (Desmognathus ocoee), a species in which female organisms store sperm for up to 9 months prior to fertilization. We found that 96% of clutches were sired by multiple males, but that the majority of females used sperm from only two or three males to fertilize their eggs. The high rate of multiple mating by females suggests that sperm competition is an important aspect of this mating system. Comparison of our data with those of other parentage studies in salamanders and newts reveals that multiple mating may be common in urodele amphibians. Nevertheless, the number of males siring offspring per clutch in D. ocoee did not differ appreciably from that in other species of urodeles with shorter storage periods.