Adult–Adult Play in Primates: Comparative Analyses of its Origin, Distribution and Evolution

Comparative analyses were conducted on a data set derived from the literature so as to test several hypotheses which were developed to explain the distribution of adult–adult play fighting within the order primates. Ratings for play occurring in sexual and non‐sexual contexts were developed. Three hypotheses were evaluated: (i) that play occurring in non‐sexual social contexts is a byproduct of its use in sex; (ii) that the occurrence of play is related to its use for social assessment and manipulation, and so is more likely to be present in species with reduced familiarity between individuals; and (iii) that phylogenetic affiliation influences the likelihood that species within clades engage in play. We used independent contrasts to test the first two hypotheses, and both were significant, with the presence of play in sexual contexts accounting for 14–16% of the variance of play in non‐sexual contexts, and reduced social familiarity accounting for 30–40% of the variance in the occurrence of play in non‐sexual contexts. To test the third hypothesis, we mapped the occurrence of both types of play onto known phylogenies. The overlap was not congruent, indicating that phylogenetic relationships did not account for the distribution of play. Given that play in both sexual and non‐sexual contexts was more likely to occur in species with a social organization involving reduced frequency of contact between the sexes and other social group members, we suggest that the likely adaptive value of play fighting is as a tool for social assessment and manipulation. The possible factors that mitigate the use of play fighting for these purposes, such as the availability of other forms of communication that could serve similar functions, are discussed.     

Sound production during courtship and spawning of Oreochromis mossambicus: male–female and male–male interactions

The role of sound production of the Mozambique tilapia Oreochromis mossambicus in agonistic and mating interactions observed during hierarchy formation and in established groups was examined. Only territorial males produced sounds, during male–female and male–male courtship interactions and during pit-related activities ( e.g. dig, hover and still in the nest). Sound production rate was positively correlated with courting rate. Although sounds in other cichlids are typically emitted in early stages of courtship, O. mossambicus produced sounds in all phases, but especially during late stages of courtship, including spawning. It is suggested that the acoustic emissions in this species may play a role in advertising the presence and spawning readiness of males and in synchronizing gamete release.     

Precocious Courtship and Play in Emydid Turtles

In many mammal species, precocious sexual behaviour is a component of play. A recent model for the evolution of play fighting behaviour in muroid rodents by Pellis (1993) proposes that social play in those species has its origin in precocious sexual behaviour. Captive juvenile emydid turtles perform precocious sexual behaviour. After reviewing its occurrence, we focus on detailed observations of Pseudemys nelsoni. Precocious sexual behaviour in these turtles is characterized by the striking ‘titillation’ display, usually observed only when adult males court females. In this display, the digits of the front feet are rapidly vibrated above the eyes of the female. In our observations, both sexes performed the display, which was energetic, spontaneous, and inconclusive (in that sequences of precocious courtship typically ended when either the displayer or recipient stopped and rested, left, or started some other unrelated non-social behaviour). Displaying individuals clearly preferred conspecific recipients and often appeared to seek out specific individuals. We discuss several plausible explanations for precocious courtship in these turtles but find none entirely satisfying. The characteristics of the precocious courtship behaviour we observed most closely match those commonly listed for social play. Thus, we conclude that the most likely explanation for this behaviour is that it is a component of social play.     

Male Siamese Fighting Fish, Betta splendens, Increase Rather than Conceal Courtship Behavior when a Rival is Present

The impact of social environment on mating success is especially pronounced in species where both intraspecific and interspecific selection influence reproduction, such as the Siamese fighting fish. Males alter male–male interactions when either a male or female audience is present, but how males change their behavior toward a female when a rival male is present is unknown. This study addresses whether males alter their behavior toward a female in a way that would prevent a rival male from interrupting courtship. The behavior of male Siamese fighting fish toward a dummy female was examined under various degrees of visual cover, both in the presence and absence of a rival male, to investigate whether males use concealment provided by the structural environment to their advantage. While males did not use barriers to conceal courtship as hypothesized, males altered their behavior by increasing courtship and monitoring their nest when a rival was visible. This increase in courtship is in contrast to most studies on courtship in the presence of a rival that find a reduction in courtship behavior. Males spent more time opercular gill flaring when no barriers were present, suggesting that males may be trying to court the female and communicate to the rival simultaneously. There was also a trend for aggression toward the female and the rival to decrease as screen length increased. Thus, males compensate for the presence of a rival by adjusting their courtship and aggressive behaviors, which could have important implications for courtship success.     

Effects of copulation temperature on female reproductive output and longevity in the wolf spider Pardosa astrigera (Araneae: Lycosidae)

The copulation duration of male wolf spider Pardosa astrigera, was significantly influenced by environmental temperature, as had been found in some insect species. Therefore, temperature during male courtship and copulation may influence the amount of sperm and seminal fluids transferred during copulation, which in turn could influence female fitness. In order to test this hypothesis, we subjected pairs of male and female P. astrigera to five temperature groups from 16 to 32 °C at an interval of 4 °C, and investigated whether and to what extent the various temperatures during male courtship and copulation influenced female reproductive output and female adult longevity under controlled laboratory conditions. With the increase of copulation temperature, females were more likely to lay egg sacs. The total egg sacs and lifetime fecundity of female were positively influenced by copulation temperature, whereas female lifetime spiderlings and adult longevity were independent of copulation temperature.     

Underwater vocalizations and associated behavior in captive ringed seals (<Emphasis Type="Italic">Pusa hispida</Emphasis>)

In pinniped species, especially those that mate in the water, acoustic communication is suggested to play an important role in various aspects of behavior. However, little is known about the behavioral context or function of vocalization, principally because direct observation is difficult in the wild. In the present study, we analyzed the seasonality, sexual differences, and behavioral contexts of the vocalizations of captive ringed seals to explore the function of such communication. The behavior of and underwater sounds made by three ringed seals (an adult male, an adult female, and a subadult female) living in Otaru Aquarium, Japan, were recorded for 19 days between August 2011 and April 2012. Six call types (long snort, knock, yelp, bark, click, and woof) were identified in the recordings. The 12 observed social behaviors could be categorized into three categories (male courtship, aggression, and submission). All call types except clicks were vocalized during social behavior. Vocalizations of all types increased during the breeding season. The long snorts were only produced by the adult male toward an adult female during his courtship behavior. All three individuals emitted knocks, yelps, and bark sounds. Of these three call types, knocks were associated with aggressive behavior or the male’s courtship behavior. In contrast, alternate series of yelps and barks were vocalized by the recipients of aggressive behaviors, suggesting their function as submissive signals. This study could be applied to the monitoring of wild ringed seals with passive acoustic recordings to assess not only their distribution but also their behavior.     

Spatial Association in a Highly Inbred Ungulate Population: Evidence of Fine-Scale Kin Recognition

We present the first evidence of fine-scale kin recognition, based on a continuous measure of relatedness, in ungulates. The spatial association between herdmates of a captive population of aoudad ( Ammotragus lervia ), where all the individuals are related, is analysed during resting time. Our goal was to estimate which factors influence individuals' associations. The study population is highly inbred, although it does not show serious deleterious effects caused by consanguinity. It comprises a single captive herd, reproducing freely and in good conditions for more than 10 yr. It emerges that kin, measured as the coefficient of relationship between two given herdmates, is the main factor determining the spatial association (e.g. average distance) of male–male and female–female dyads, as more-related individuals tend to rest closer to each other than less-related ones. As for male–female dyads, individuals of a similar age tend to stay closer. To rule out any familiarity confounding effects, individuals' cohabitation time in the herd was added as a random factor in the analyses. Concerning the type of dyad, mother–calf dyads are characterized by higher proximity than others, particularly during the suckling period, whereas males tend to stay closer to each other than females or male–female dyads, being also more kin-related. Female social rank does not influence spatial association between herdmates. These results are related to group composition of the species in the wild, which are characterized by intense mother–calf bonds and all-male groups that are probably kin-related. It is seen that adult male–female associations are not related to kinship, but to age similarity, which is in accord with the assumption that main family groups in the wild are formed by matrilineal lines, whereas males are the dispersing sex.     

Strong Competition Does Not Always Predict Play Asymmetry: The Case of South American Sea Lions (Otaria flavescens)

Although play fighting has been studied for over a century in both human and non‐human animals, quantitative data on marine mammals are still scarce. Here, we investigated play fighting in South American sea lions (Otaria flavescens), one of the most sexually dimorphic species with an extreme polygynous mating system, high levels of both intra‐ and inter‐sexual competition. All these features make South American sea lions a good model species to test some predictions on play fighting. Our results indicate play is restricted to juveniles, being inhibited among adults, and as to be expected in a species that shows a high degree of sexual dimorphism, it is mainly expressed in males. Even though playful interactions were punctuated by competitive behaviours, animals played in a highly symmetric way and were able to adjust their competitive playful interactions in a flexible manner and so reduce the risk of escalation to a minimum level. They were highly selective in their choice of playmates by limiting the number of players per session and playing more with age‐matched companions and friends. All these factors taken together are probably at the basis of the low risk of escalation recorded during the study. This result is predictive of a high ability and motivation of these animals to engage in play behaviour which can have a possible role not only in the acquisition of dominance status, but also in establishing and maintaining social relationships, an unexpected role in a so highly competitive species.     

Analysis of tufted capuchin (Cebus apella) courtship and sexual behavior repertoire: changes throughout the female cycle and female interindividual differences

Sexual solicitations and initiative (proceptivity, sensu Beach [1976] Horm Behav 7:105-138) are important components of the sexuality of females of many primate species. In the tufted capuchin (Cebus apella), female proceptivity characterizes the species' mating system. In study 1, we defined and discussed 20 behavioral patterns based on the observation of 6 females and 5 males living in two social groups. In study 2, each behavior, including mounting activity, was quantitatively assessed during the periovulatory and nonperiovulatory cycle phases of 4 females, detected on the basis of urinary progestin levels (N = 20 ovulatory cycles, 5 for each female); moreover, we monitored changes in females' social interactions (agonism, grooming activity, and play). Nine of the behaviors typically used by the female during courtship and in sexual interactions showed a dramatic increase during the periovulatory phase. Though males mounted females at an apparently higher rate during the periovulatory than the nonperiovulatory phase, the difference was not significant. However, when adult male mounting is separated into those which occur within play and nonplay contexts, there is a significant periovulatory phase effect for mounts not associated with play. Females groomed adult males at the same rate throughout the cycle. Agonism and play did not show any phase effect; however, females' avoidance of adult males significantly increased during the periovulatory phase. Finally, each female made a statistically different use of the behavioral repertoire by performing some behaviors more than others. This variability among females during courtship calls for further research into whether it affects mating success.     

Temporal and Spatial Distribution of Male Scent Marks in the Polygynous Greater Sac-Winged Bat

Scent marks are relatively long-lived signals that can be perceived by conspecifics when the producer is absent. Therefore, it is often not obvious to whom the signal is directed. In daytime roosts of the polygynous greater sac-winged bat, males scent mark territories with facial gland secretions. Territories are a valuable resource for males, as they offer exclusive courtship opportunities, which results in increased male reproductive success and, consequently, increased male–male competition over territories. The information encoded in male scent marks could, therefore, be either directed at females as part of an olfactory courtship display or at male competitors as part of territorial behaviour. We expected territorial males to scent mark in the morning, shortly before females return to the territory and close to female roosting sites, if scent marks are directed at females as part of the courtship display. And we expected harem males to scent mark at the territory boundaries, where male–male encounters are most likely to occur, if scent marks are directed at male competitors. We found that males marked more frequently in the afternoon, at a time when all females have already left the territory, and harem males marked at the territory boundaries and not inside their territory in the area where females roost. At boundaries males fan volatiles from specialised wing sacs towards competitors outside the territory. Scent marking of male Saccopteryx bilineata might therefore be congruent with the assessment-hypothesis, which states that scent marks offer intruders the possibility to make an olfactory assessment of the territory owner without direct physical interaction. Thus, scent marks of male S. bilineata are most likely influenced by male–male competition and not by female choice.     

Female control in yellow-legged gulls: trading paternity assurance for food

Females in many socially monogamous birds copulate hundreds of times more than necessary for fertilization, although little is known about the benefits of this excess. Females may not directly benefit from high copulation rates, but instead may exploit male interest in copulating to obtain benefits. In species with courtship feeding, females may trade copulations for food (immediate benefits hypothesis). I tested this hypothesis by analysing female behaviour during courtship in yellow-legged gulls, Larus cachinnans. Female gulls to some extent controlled sperm transfer, because they moved during copulation bouts, and this behaviour influenced the number of cloacal contacts per mounting that the male achieved. Female control was related to previous feeding by the male, and hence the male courtship feeding rate correlated with the cloacal contact rate. Males that give more food probably enhance their chances of fathering offspring. By analysing within-individual female behaviour, I also found that the number of cloacal contacts was higher when the male fed the female than when he did not, which indicates that female gulls followed a decision rule to resist copulation when food is not given. Overall, these results support the hypothesis that female gulls manipulate their mates to obtain food.     

Male Performance and Body Size Affect Female Re-Mating Occurrence in the Orb-Web Spider Leucauge mariana (Araneae, Tetragnathidae)

Females can affect male probabilities of paternity success through behavioural, morphological and/or physiological processes occurring during or after copulation. These processes under female-control include the acceptance or rejection of mating attempts by subsequent males. Leucauge mariana is an orb weaving spider that shows male mate guarding of penultimate females, male–male competition on female webs and copulatory plugs, suggesting a polyandric mating system. The aim of the present study was to ascertain whether male behaviour during courtship and copulation in L. mariana relate with female re-mating decisions. Forty-three virgin females were exposed to up to three males until they mated. In 24 cases, the copulatory plug was absent after mating and females were exposed the next day to up to three other males. Eighteen females accepted a second mating. Relatively larger females were more receptive to second matings and were more likely to copulate if the second male was smaller. Longer duration of female tapping and abdominal bobbing during courtship, and first copulations with less short insertions and more flubs, were associated with increased female acceptance to second matings. The results indicate cryptic female choice on male courtship and copulatory performance and suggest female-control over the determination of male mating success in this spider species.     

Social Play among Juvenile Bighorn Sheep: Structure,Development, and Relationship to Adult Behavior

A 27-mo study of bighorn sheep (Ovis canadensis) was conducted to examine the structure and development of social play among lambs, and to compare that behavior with the behavior of yearlings and adults. Male lambs played more than females and exhibited a larger repertoire. The behavior patterns used by lambs in social play were the same as those used by adults in intrasexual conflict and courtship. However, the repertoire of lambs was more limited than that of adults. Lambs chose partners closest in age to interact with, regardless of sex. Results were consistent with the hypothesis that play serves to develop physical skills and strength.     

Sexual behaviour of immature male eastern mosquitofish: a way to measure intensity of intra-sexual selection?

Immature males of eastern mosquitofish Gambusia holbrooki start to be sexually active well before their copulatory organ (gonopodium) has completely developed and before they become able to transfer sperm. Sexual activity of males, consisting of copulatory attempts tending to bypass female acceptance, is intense (one attempt per minute) and is likely to be energetically very costly. The sexual behaviour of immature males relative to their maturation stage is described and tested against two possible adaptive explanations. Sexual activity was present in males from the beginning of the development of their gonopodium and increased during the following stages of maturation. Two to three weeks before gonopodium development was completed, sexual activity of immatures was as high as that of adults. Adult males showed aggressive behaviour against a male attempting a copulation, irrespective of the maturity of the latter. Since previous studies have shown that the reproductive success in this species is negatively correlated with male size when male–male competition is low (i.e. when the sex ratio is female biased), but decreases with male size when competition is high, the hypothesis was tested that sexual activity of immature males functions as a way to predict their future reproductive success if they mature at a given size. A second hypothesis tested was that precocious sexual experience improves the efficiency of copulatory attempts. Results were more in agreement with the first hypothesis, since size at maturity of males was influenced by the sex ratio experienced during maturation and precocious experience gave very little advantage.     

Courtship Disruption at the Lek in the Guianan Cock-of-the-Rock

During 4 seasons of study at a large (55 male) lek of Guianan cock-of-the-rock (Rupicola rupicola) in Suriname, we observed 3906 female courtship visits. Of these, 1171 (30.0%) were disrupted by adult males, 430 (11.0%) were disrupted by yearling males, and 289 (7.4%) were disrupted by females. This is one of the highest levels of courtship disruption reported among lek-breeding birds. Disruption was performed by approximately half of the territorial adult males each year, spanning the full range of mating success and territory location. Courtship disruption occurs in two contexts among adult male cock-of-the-rock. The most frequently performed disruptions were low-intensity supplantings and threats directed toward more successful territorial neighbors. These appear to reflect attempts to improve or maintain territorial status within the male social organization. Less commonly, individual males persistently directed high-intensity disruption toward specific females. Such males succeeded in redirecting the females' mate choice to themselves in 27% of instances. We found no support for the hypothesis that females choose males on the basis of their immunity to disruption. Reproductively successful males received disruption at proportionately equal or greater levels than unsuccessful males. Courtship disruption by yearling cock-of-the-rock occurred primarily in the context of practice courtship by these non-territorial immatures. Disruption by females was uncommon and did not appear to deny or even delay access to any male. We discuss these results in the light of recent proposals concerning the role of courtship disruption in the operation of mate choice and the determination of male dispersion on leks.     

Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IX. Host plant and population specific epicuticular hydrocarbon expression influences mate choice and sexual selection

Sexual signals in cactophilic Drosophila mojavensis include cuticular hydrocarbons (CHCs), contact pheromones that mediate female discrimination of males during courtship. CHCs, along with male courtship songs, cause premating isolation between diverged populations, and are influenced by genotype × environment interactions caused by different host cacti. CHC profiles of mated and unmated adult flies from a Baja California and a mainland Mexico population of D. mojavensis reared on two host cacti were assayed to test the hypothesis that male CHCs mediate within‐population female discrimination of males. In multiple choice courtship trials, mated and unmated males differed in CHC profiles, indicating that females prefer males with particular blends of CHCs. Mated and unmated females significantly differed in CHC profiles as well. Adults in the choice trials had CHC profiles that were significantly different from those in pair‐mated adults from no‐choice trials revealing an influence of sexual selection. Females preferred different male CHC blends in each population, but the influence of host cactus on CHC variation was significant only in the mainland population indicating population‐specific plasticity in CHCs. Different groups of CHCs mediated female choice‐based sexual selection in each population suggesting that geographical and ecological divergence has the potential to promote divergence in mate communication systems.     

Ontogeny of sexual dimorphism in the Long-tailed Manakin Chiroxiphia linearis: long maturation of display trait morphology

Males of dimorphic species often show ornaments that are thought to have evolved through female choice or/and male–male competition. The sexual differentiation of similar morphologies occurs during ontogeny, resulting in differential sex and age-specific selection. The Long-tailed Manakin is a dimorphic species with a highly skewed mating system, the males of which delay plumage maturation over 3 to 4 years. We describe ontogenetic changes in feather morphology in this species through sexual maturity. Males showed a significant increase in length of the central rectrices with age, hence their degree of sexual dimorphism increased from zero in 1-year-old males to 189.5% in adults. In contrast, male tail length decreased with age. Wing length did not vary significantly with age, but females had relatively longer wings than males. Wing loading was greater in females and decreased with age in males. In adults, rectrix length was positively correlated with testis volume, supporting the hypothesis that secondary sexual characters can signal the condition of primary sexual characters. Rectrix length showed positive allometry with body size in males less than 4 years old, whereas older males showed negative allometry and females showed isometry. Wing area and wing loading shifted from negative to positive allometry in males of 2 to 3 years of age. Changes in male morphology during ontogeny in the Long-tailed Manakin appeared to be associated with their specific display behaviours. Age-related changes in allometric growth of rectrices in the Long-tailed Manakin suggested that young males invest disproportionately more in the length of this trait relative to their body size. This investment could act as a signal of competitive ability to move status position in their orderly queue.     

The Right Time to Happen: Play Developmental Divergence in the Two Pan Species

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a ‘timing hotspot’ for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.     

Female presence and estrous state influence mouse ultrasonic courtship vocalizations

The laboratory mouse is an emerging model for context-dependent vocal signaling and reception. Mouse ultrasonic vocalizations are robustly produced in social contexts. In adults, male vocalization during courtship has become a model of interest for signal-receiver interactions. These vocalizations can be grouped into syllable types that are consistently produced by different subspecies and strains of mice. Vocalizations are unique to individuals, vary across development, and depend on social housing conditions. The behavioral significance of different syllable types, including the contexts in which different vocalizations are made and the responses listeners have to different types of vocalizations, is not well understood. We examined the effect of female presence and estrous state on male vocalizations by exploring the use of syllable types and the parameters of syllables during courtship. We also explored correlations between vocalizations and other behaviors. These experimental manipulations produced four main findings: 1) vocalizations varied among males, 2) the production of USVs and an increase in the use of a specific syllable type were temporally related to mounting behavior, 3) the frequency (kHz), bandwidth, and duration of syllables produced by males were influenced by the estrous phase of female partners, and 4) syllable types changed when females were removed. These findings show that mouse ultrasonic courtship vocalizations are sensitive to changes in female phase and presence, further demonstrating the context-sensitivity of these calls.     

Getting that female glance: Patterns and consequences of male nonverbal behavior in courtship contexts

Females apparently are the choosier sex in courtship contexts, but there still is limited information about female selection criteria in real courtship settings. Given that a female knows little about a heretofore unacquainted male, upon what dimensions can (and do) females base their initial courtship decisions? Here, we report findings from observational studies that investigated male nonverbal behavior in a bar context. Study 1 documented the body movements of males prior to making contact with a female. It was found that males who successfully made “contact” courtship initiation with females exhibited different body language in this precontact phase than did males who did not make contact with females, including significantly more glancing behaviors, space-maximization movements, intrasexual touching, and less closed-body movements. The findings from a second within-subject study comparing the behavior of men in a bar when women were present or not present supported the initial study's findings and showed that males' emphasis on these behaviors increases in a mate-relevant context. We suggest that certain aspects of male nonverbal behavior in courtship contexts can serve as self-presentation and mate-value signals.