Body signals used during social play in captive immature western lowland gorillas

The play face is a well-established play signal in nonhuman primates that functions to invite play and convey a playful intent. However, recent evidence indicates that some species display repertoires of play signals that may have more specific meanings related to particular aspects of play. Furthermore, previous studies have inconsistently categorized gorilla behaviors as play signals versus actual play. Here we aim to identify behaviors displayed by two immature captive western lowland gorillas (Gorilla gorilla gorilla) at the Buffalo Zoo that meet three necessary criteria to be considered play signals. Specifically, we (1) investigate whether 21 candidate signals are significantly different from actual play behaviors, (2) and from similar signals used in non-play contexts, and (3) determine whether they predict the occurrence of social play. The results indicate that at least 18 of the 21 candidate signals have strong support for classification as play signals. These findings represent first steps in determining the function of multiple play signals in gorillas.     

The ontogeny of play in feral olive baboons (Papio anubis)

Behaviours that always appear playful (play markers) are distinguished from behaviours that appear playful in some contexts, but not others (context-dependent play components). Age changes in the frequency of performance of both kinds of playful behaviours are described, as are age changes in the frequency with which context-dependent play components accompany play markers in baboon social interactions. Some quantitative properties of social interactions containing and lacking play markers are compared. Interactions with play markers last longer and have a higher rate of change of constituent behaviours than interactions without. Animals are also more persistent in the face of changes in their partner's behaviour in interactions with play markers. It is suggested that an attempt to produce a definition of play is not a useful enterprise, but that it is important to investigate causal mechanisms underlying behaviours that appear playful to human observers, and to clarify the relationships among those mechanisms. Data are presented suggesting that at least two sets of mechanisms, not totally separate, underly the performance of baboon social play. Functions of the behaviours controlled by these mechanisms are discussed.     

Foster carers influence brood pathogen resistance in ants

Social organisms face a high risk of epidemics, and respond to this threat by combining efficient individual and collective defences against pathogens. An intriguing and little studied feature of social animals is that individual pathogen resistance may depend not only on genetic or maternal factors, but also on the social environment during development. Here, we used a cross-fostering experiment to investigate whether the pathogen resistance of individual ant workers was shaped by their own colony of origin or by the colony of origin of their carers. The origin of care-giving workers significantly influenced the ability of newly eclosed cross-fostered Formica selysi workers to resist the fungal entomopathogen Beauveria bassiana. In particular, carers that were more resistant to the fungal entomopathogen reared more resistant workers. This effect occurred in the absence of post-infection social interactions, such as trophallaxis and allogrooming. The colony of origin of eggs significantly influenced the survival of the resulting individuals in both control and pathogen treatments. There was no significant effect of the social organization (i.e. whether colonies contain a single or multiple queens) of the colony of origin of either carers or eggs. Our experiment reveals that social interactions during development play a central role in moulding the resistance of emerging workers.     

Welcome Back: Responses of Female Bonobos (Pan paniscus) to Fusions

In species with a high degree of fission-fusion social dynamics, fusions may trigger social conflict and thus provide an opportunity to identify sources of social tension and mechanisms related to its alleviation. We characterized behavioral and endocrine responses of captive female bonobos (Pan paniscus) to fusions within a zoo facility designed to simulate naturalistic fission-fusion social dynamics. We compared urinary cortisol levels and frequencies of aggression, grooming and socio-sexual interactions between female bonobos while in stable sub-groups and when one “joiner” was reunited with the “residents” of another sub-group. We hypothesized that fusions would trigger increases in aggression and cortisol levels among reunited joiners and resident females. We further predicted that females who face more uncertainty in their social interactions following fusions may use grooming and/or socio-sexual behavior to reduce social tension and aggression. The only aggression on reunion days occurred between reunited females, but frequencies of aggression remained low across non-reunion and reunion days, and there was no effect of fusions on cortisol levels. Fusions did not influence patterns of grooming, but there were increases in socio-sexual solicitations and socio-sexual interactions between joiners and resident females. Joiners who had been separated from residents for longer received the most solicitations, but were also more selective in their acceptance of solicitations and preferred to have socio-sexual interactions with higher-ranking residents. Our results suggest that socio-sexual interactions play a role in reintegrating female bonobos into social groups following fusions. In addition, females who receive a high number of solicitations are able to gain more control over their socio-sexual interactions and may use socio-sexual interactions for other purposes, such as to enhance their social standing.     

A motivational analysis of object play in juvenile dwarf mongooses (Helogale undulata rufula)

The dwarf mongoose (Helogale undulata rufula) has a play vocalization, a short pulse at the 2-kHz level which is repeated at a rate of 3 to 12 or more pulses/s during the entire play period. The repetition rate is indicative of motivation intensity. This motivational study on object play shows that: (1) play becomes fragmented prior to termination; (2) motivation changes during a session fall into three different patterns all terminating at a ‘set point’ or ‘sollwert’; (3) the behaviour patterns performed during play show little sequencing related to original context but are causally different from those of exploration and have ‘optimum intensities’; (4) more limbs employed in object manipulation indicate higher intensity irrespective of the original non-play context of the behaviour pattern concerned; and (5) high intensity is coupled with more behaviour patterns performed per time interval. Hand-reared isolates show a delay in the appearance of play in ontogeny in comparison with pair-raised animals and their play contains a higher frequency of patterns bringing the object into close bodily contact. Play is considered as being a behaviour pattern complex with its own motivation which, through its performance, may compensate for motivational deficits or surpluses, a set point or sollwert replacing a consummatory act. Behaviour patterns from other behavioural contexts are taken over and reordered with regard to different rules, hence the apparent lack of sequencing. A threshold of general excitation associated with stimulus input is postulated as regulating the time of appearance of play in ontogeny, not maturational factors, and it may be used to compensate for specific stimulatory deficits occurring during ontogeny.     

Social play does not reduce aggression in wild meerkats

Of the numerous hypotheses advanced to explain the adaptive significance of play, several assert that social play increases social harmony, cementing alliances and reducing aggression between group members or littermates. These hypotheses are frequently cited, but their validity remains unknown. We examined the relation between social play and aggression in juvenile meerkats, Suricata suricatta, living in a wild population in the southern Kalahari Desert. We tested the hypothesis that social play reduces aggression, by examining rates of play, play partner choices, the structure of social play and rates of aggressive interactions during foraging. We found no relation between frequency of play and level of aggression, either between individuals or during the course of development. Pups that played together frequently were just as aggressive towards one another as pairs of pups that played infrequently, and play interactions had no subsequent effect on the likelihood of aggression. In contrast, aggressive interactions during foraging inhibited the subsequent likelihood of play, and high levels of aggression during foraging changed the structure of social play, with victimized pups avoiding play wrestling. We conclude that social play does not reduce aggression in young meerkats. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Social play in the development of sibling relations in Eurasian lynx (Lynx lynx)

Social play fulfills an important function in creating and maintaining relations between siblings. However, its relationship with the intralitter social processes is poorly understood. It was noticed that, in Eurasian lynx (Lynx lynx) litters, sex differences in social play are absent in the first 2–3 months of life. It was found that the most intense periods of play behavior (at an age of 9 and 12 weeks) coincide with periods of aggression. Gradual change in play interactions, which require close physical contact by play elements with increased motor activity, are described. This reflects the changes in the relevance of certain skills of lynx cubs as they grow older.     

Anxiety-related behavior of orphan chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania

This study examined the anxiety levels and social interactions of two orphan and four mother-reared adolescent chimpanzees (Pan troglodytes schweinfurthii) in the Kasekela community at Gombe National Park, Tanzania. We used focal sampling in the field at Gombe to observe these adolescent individuals. Their social interactions and anxious behavior, measured as rough scratching, were recorded. The two orphans differed from others of a similar age by exhibiting higher levels of anxiety and lower levels of play. These results suggest that a mother’s absence, even in naturalistic conditions in which other members of the community are available to the orphan, may have long-lasting impact on an adolescent’s anxiety and its ability to engage in complex social interactions, such as play.     

Early play may predict later dominance relationships in yellow-bellied marmots (Marmota flaviventris)

Play has been defined as apparently functionless behaviour, yet since play is costly, models of adaptive evolution predict that it should have some beneficial function (or functions) that outweigh its costs. We provide strong evidence for a long-standing, but poorly supported hypothesis: that early social play is practice for later dominance relationships. We calculated the relative dominance rank by observing the directional outcome of playful interactions in juvenile and yearling yellow-bellied marmots (Marmota flaviventris) and found that these rank relationships were correlated with later dominance ranks calculated from agonistic interactions, however, the strength of this relationship attenuated over time. While play may have multiple functions, one of them may be to establish later dominance relationships in a minimally costly way.     

Social facilitation of insect reproduction with motor-driven tactile stimuli

Tactile stimuli provide animals with important information about the environment, including physical features such as obstacles, and biologically relevant cues related to food, mates, hosts and predators. The antennae, the principal sensory organs of insects, house an array of sensory receptors for olfaction, gustation, audition, nociception, balance, stability, graviception, static electric fields, and thermo-, hygro- and mechanoreception. The antennae, being the anteriormost sensory appendages, play a prominent role in social interactions with conspecifics that involve primarily chemosensory and tactile stimuli. In the German cockroach (Blattella germanica) antennal contact during social interactions modulates brain-regulated juvenile hormone production, ultimately accelerating the reproductive rate in females. The primary sensory modality mediating this social facilitation of reproduction is antennal mechanoreception. We investigated the key elements, or stimulus features, of antennal contact that socially facilitate reproduction in B. germanica females. Using motor-driven antenna mimics, we assessed the physiological responses of females to artificial tactile stimulation. Our results indicate that tactile stimulation with artificial materials, some deviating significantly from the native antennal morphology, can facilitate female reproduction. However, none of the artificial stimuli matched the effects of social interactions with a conspecific female.     

Pattern of play behavior in infant (age 1 to 12 months) white‐headed langurs in limestone forests,southwest China

Play behavior is a significant trait of immature nonhuman primates (hereafter primates) that plays an important role in sensory, locomotor, socio‐cognitive, and developmental processes. It has been suggested that the function of play is to practice and improve motor skills related to foraging, avoiding predators, attracting mates, raising offspring, and strengthening the skills needed for the formation and maintenance of social bonds. From September 2009 to August 2010, we investigated the play behavior of 1–12 month‐old infant white‐headed langurs (Trachypithecus leucocephalus) a Critically Endangered primate species endemic to China. We carried out this study in the Guangxi Chongzuo White‐headed Langur National Nature Reserve, and recorded 4421 play bouts and 1302 min of play engaged in by seven infants. We found that infants of different ages exhibited different patterns of play behavior. Specifically, nonsocial play behaviors appeared at one month of age, social play behaviors at two months, and an expanded repertoire of social and non‐social play behaviors at three months of age. The frequency and duration of nonsocial play peaked at five months of age and then decreased, while social play gradually increased with age. Nonsocial play did not differ between the sexes, whereas social play showed sex specificity, with a higher frequency and longer duration of social play in male infants compared to female infants. In addition, male and female white‐headed langur infants appeared to prefer individuals of same sex as social playmates, but no obvious choice preference for a specific individual. In conclusion, we provide the first report of play behavior in a population of wild Critically Endangered white‐headed langurs. We suggest that age‐ and sex‐specific differences in play behavior of infants form the bases for age and sex‐based differences in the social interactions of adult langurs.     

Effects of social environment on baseline glucocorticoid levels in a communally breeding rodent,the colonial tuco-tuco (Ctenomys sociabilis)

The social environment in which an animal lives can profoundly impact its physiology, including glucocorticoid (GC) responses to external stressors. In social, group-living species, individuals may face stressors arising from regular interactions with conspecifics as well as those associated with basic life history needs such as acquiring food or shelter. To explore the relative contributions of these two types of stressors on glucocorticoid physiology in a communally breeding mammal, we characterized baseline GC levels in female colonial tuco-tucos (Ctenomys sociabilis), which are subterranean rodents endemic to southwestern Argentina. Long-term field studies have revealed that while about half of all yearling female C. sociabilis live and breed alone, the remainder live and breed within their natal group. We assessed the effects of this intraspecific variation in social environment on GC physiology by comparing concentrations of baseline fecal corticosterone metabolite (fCM) for (1) lone and group-living yearling females in a free-living population of C. sociabilis and (2) captive yearling female C. sociabilis that had been experimentally assigned to live alone or with conspecifics. In both cases, lone females displayed significantly higher mean baseline fCM concentrations. Data from free-living animals indicated that this outcome arose from differences in circadian patterns of GC production. fCM concentrations for group-living animals declined in the afternoon while fCM in lone individuals did not. These findings suggest that for C. sociabilis, stressors associated with basic life history functions present greater challenges than those arising from interactions with conspecifics. Our study is one of the first to examine GC levels in a plural-breeding mammal in which the effects of group-living are not confounded by differences in reproductive or dominance status, thereby generating important insights into the endocrine consequences of group-living.     

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

A descriptive study of social development in the rat (Rattus norvegicus)

The social interactions between juvenile rat pups (Rattus norvegicus) were observed daily between 21 and 55 days of age. The data were analysed for developmental changes, sex differences, play-partner preferences, and dominance relations. The results revealed clear patterns in the development of sexual and agonistic behaviours in the rat. This development refers to changes in either the manner in which animals interact or the behaviours involved in social play, but not to the topography of specific behaviours. Development toward the adult pattern of social behaviour was temporally associated with the period of sexual maturation (i.e. between days 36 and 50).     

Individual differences in the ability to recognise facial identity are associated with social anxiety

Previous research has been concerned with the relationship between social anxiety and the recognition of face expression but the question of whether there is a relationship between social anxiety and the recognition of face identity has been neglected. Here, we report the first evidence that social anxiety is associated with recognition of face identity, across the population range of individual differences in recognition abilities. Results showed poorer face identity recognition (on the Cambridge Face Memory Test) was correlated with a small but significant increase in social anxiety (Social Interaction Anxiety Scale) but not general anxiety (State-Trait Anxiety Inventory). The correlation was also independent of general visual memory (Cambridge Car Memory Test) and IQ. Theoretically, the correlation could arise because correct identification of people, typically achieved via faces, is important for successful social interactions, extending evidence that individuals with clinical-level deficits in face identity recognition (prosopagnosia) often report social stress due to their inability to recognise others. Equally, the relationship could arise if social anxiety causes reduced exposure or attention to people's faces, and thus to poor development of face recognition mechanisms.     

Rapid Decision-Making with Side-Specific Perceptual Discrimination in Ants

Background

Timely decision making is crucial for survival and reproduction. Organisms often face a speed-accuracy trade-off, as fully informed, accurate decisions require time-consuming gathering and treatment of information. Optimal strategies for decision-making should therefore vary depending on the context. In mammals, there is mounting evidence that multiple systems of perceptual discrimination based on different neural circuits emphasize either fast responses or accurate treatment of stimuli depending on the context.

Methodology/Principal Findings

We used the ant Camponotus aethiops to test the prediction that fast information processing achieved through direct neural pathways should be favored in situations where quick reactions are adaptive. Social insects discriminate readily between harmless group-members and dangerous strangers using easily accessible cuticular hydrocarbons as nestmate recognition cues. We show that i) tethered ants display rapid aggressive reactions upon presentation of non-nestmate odor (120 to 160 ms); ii) ants'' aggressiveness towards non-nestmates can be specifically reduced by exposure to non-nestmate odor only, showing that social interactions are not required to alter responses towards non-nestmates; iii) decision-making by ants does not require information transfer between brain hemispheres, but relies on side-specific decision rules.

Conclusions/Significance

Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition. We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates. This asks for a reappraisal of the mechanisms underlying social recognition in insects.     

Homosexual behaviour and female-male mounting in mammals—a first survey

Information from the literature is given on the presence or absence of homosexual behaviour and female-male mounting in 125 species of mammals, both captive and wild. Such behaviour occurs in the male and often female young of many species soon after their birth. It is more common in young, often in play, than in adults. Adult homosexual behaviour is widespread in male and female mammals (recorded in 63 and 71 species respectively), but common in few species. In males it is most likely to be correlated with dominance and thus to occur in species with hierarchies such as terrestrial monkeys and members of the sheep and goat tribe. In females it is often correlated with sexual condition; a female in heat most often mounted another female, and one in heat was next most likely to be mounted by another female. Anoestral females rarely mounted other anoestral females. Females of 43 species mounted males, which often excited them sexually. Captive mammals tended to mount animals of the same sex more often than did wild ones when comparative data were available. Domestic animals also mounted more man did wild ones, with several exceptions. Some phylogenetic groups of animals displayed similar degrees of homosexual mounting, but there was often considerable variation between closely related species. Nor could homosexual mounting be always correlated with the social structure of a group. The four reasons for, or contexts of, homosexual and female-male mountings were social play (in 34 species), aggression (19 species), sexual excitement (36 species), and physical contact—non-play (30 species). This last category included a state of tension, getting attention, greeting, grooming, caressing, reassurance and appeasement. There was some overlap between categories. Homosexual pair-bonds occur in captive mammals and have been observed throughout the year in non-captive female Japanese monkeys.     

Lipsmacking Imitation Skill in Newborn Macaques Is Predictive of Social Partner Discrimination

Newborn rhesus macaques imitate facial gestures even after a delay, revealing the flexible nature of their early communicative exchanges. In the present study we examined whether newborn macaques are also sensitive to the identities of the social partners with whom they are interacting. We measured infant monkeys'' (n = 90) lipsmacking and tongue protrusion gestures in a face-to-face interaction task with a human experimenter in the first week of life. After a one-minute delay, the same person who previously presented gestures or a different person returned and presented a still face to infants. We had two primary predictions: (1) infants would demonstrate higher rates of overall gesturing, and especially lipsmacking—an affiliative gesture—to a familiar person, compared to a novel person, and (2) infants'' imitative skills would positively correlate with gestures to familiar, but not unfamiliar, social partners, as both abilities may reflect a strong general social interest. We found that overall infants did not produce more gestures or more lipsmacking when approached by a familiar person compared to a novel person; however, we did find individual differences in infants'' social responsiveness: lipsmacking imitation was positively correlated with lipsmacking during the return period when the person was the same (p = .025), but not when the person was novel (p = .44). These findings are consistent with the notion that imitative skill is reflective of infants'' more general interest in social interactions.     

Feeling Bad and Looking Worse: Negative Affect Is Associated with Reduced Perceptions of Face-Healthiness

Some people perceive themselves to look more, or less attractive than they are in reality. We investigated the role of emotions in enhancement and derogation effects; specifically, whether the propensity to experience positive and negative emotions affects how healthy we perceive our own face to look and how we judge ourselves against others. A psychophysical method was used to measure healthiness of self-image and social comparisons of healthiness. Participants who self-reported high positive (N = 20) or negative affectivity (N = 20) judged themselves against healthy (red-tinged) and unhealthy looking (green-tinged) versions of their own and stranger’s faces. An adaptive staircase procedure was used to measure perceptual thresholds. Participants high in positive affectivity were un-biased in their face health judgement. Participants high in negative affectivity on the other hand, judged themselves as equivalent to less healthy looking versions of their own face and a stranger’s face. Affective traits modulated self-image and social comparisons of healthiness. Face health judgement was also related to physical symptom perception and self-esteem; high physical symptom reports were associated a less healthy self-image and high self-reported (but not implicit) self-esteem was associated with more favourable social comparisons of healthiness. Subject to further validation, our novel face health judgement task could have utility as a perceptual measure of well-being. We are currently investigating whether face health judgement is sensitive to laboratory manipulations of mood.