Gaze direction and request gesture in social interactions

One of the most important faculties of humans is to understand the behaviour of other conspecifics. The present study aimed at determining whether, in a social context, request gesture and gaze direction of an individual are enough to infer his/her intention to communicate, by searching for their effects on the kinematics of another individual's arm action. In four experiments participants reached, grasped and lifted a bottle filled of orange juice in presence of an empty glass. In experiment 1, the further presence of a conspecific not producing any request with a hand and gaze did not modify the kinematics of the sequence. Conversely, experiments 2 and 3 showed that the presence of a conspecific producing only a request of pouring by holding the glass with his/her right hand, or only a request of comunicating with the conspecific, by using his/her gaze, affected lifting and grasping of the sequence, respectively. Experiment 4 showed that hand gesture and eye contact simultaneously produced affected the entire sequence. The results suggest that the presence of both request gesture and direct gaze produced by an individual changes the control of a motor sequence executed by another individual. We propose that a social request activates a social affordance that interferes with the control of whatever sequence and that the gaze of the potential receiver who held the glass with her hand modulates the effectiveness of the manual gesture. This paradigm if applied to individuals affected by autism disorder can give new insight on the nature of their impairment in social interaction and communication.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis

As compared with other primates, humans have especially visible eyes (e.g., white sclera). One hypothesis is that this feature of human eyes evolved to make it easier for conspecifics to follow an individual's gaze direction in close-range joint attentional and communicative interactions, which would seem to imply especially cooperative (mututalistic) conspecifics. In the current study, we tested one aspect of this cooperative eye hypothesis by comparing the gaze following behavior of great apes to that of human infants. A human experimenter "looked" to the ceiling either with his eyes only, head only (eyes closed), both head and eyes, or neither. Great apes followed gaze to the ceiling based mainly on the human's head direction (although eye direction played some role as well). In contrast, human infants relied almost exclusively on eye direction in these same situations. These results demonstrate that humans are especially reliant on eyes in gaze following situations, and thus, suggest that eyes evolved a new social function in human evolution, most likely to support cooperative (mututalistic) social interactions.     

European starlings recognize the location of robotic conspecific attention

Looking where others are allocating attention can facilitate social interactions by providing information about objects or locations of interest. We asked whether European starlings follow the orientation behaviour of conspecifics owing to their highly gregarious behaviour. Starlings reoriented their attention to follow that of a robot around a barrier more often than when the robot''s attention was directed elsewhere. This is the first empirical evidence of reorienting in response to conspecific attention in a songbird. Starlings may use this behaviour to obtain fine-tuned spatial information from conspecifics (e.g. direction of predator approach, spatial location of food patches), enhancing group cohesion.     

Communicative contexts of the LEN facial expression of pigtailed macaques (<Emphasis Type="Italic">Macaca nemestrina</Emphasis>)

We have investigated the contexts of the LEN (lips forward–ears back–neck extended) or pucker, a species-specific facial expression of Macaca nemestrina, in four breeding groups. Using the behavior sampling method we recorded all LENs, associated behavior, and the identities of the individuals involved. Of 401 LENs initiated, 62% were directed to the observer, who never responded to them in any way. Infants and dams directed more LENs to the observer than did sires or other females. The average intraspecific LEN rate was 0.82 per monkey-hour, including LENs given in reciprocation. Excluding LENs given in reciprocation, sires LENned significantly more often to females and dams than to infants, and significantly more than females and dams LENned to them. Of LENs directed to conspecifics, 21% were reciprocated, 34% were followed by distance reduction, and 16% led to both. Reciprocating LEN responses occurred more often to LENs initiated by sires. Although primarily affiliative, some LENs occurred in agonistic contexts, suggesting a possible appeasing function or rejection of a LEN’s social invitation. Aggression preceded 8% of conspecific LENs, and 15% of LENs were responded to by visual aggression. No response followed 47% of LENs. Affirming the conclusions of others, LENs are often directed by males to females before mating. LENs directed at cradled infants suggest that maternal LENs serve more than a summoning function. LENs directed to people by M. nemestrina usually seem to be inviting interaction or attention, but LENs by dams seem to reflect concerns over their infants. We speculate that at the most basic level the LEN emphasizes that the sender’s gaze is fixed on the receiver. We propose that the LEN may have evolved in this quiet rainforest species to facilitate coordination of social activity when silence or stealth is advantageous.     

Interactions between Males of the Lizard Liolaemus tenuis: Roles of Familiarity and Memory

For territorial organisms, recognition of familiar individuals can reduce the frequency and intensity of aggressive encounters (‘dear enemy’ phenomenon), stabilize social systems, and reduce the cost of territory maintenance. Here, we investigated the behavioural events displayed during contests between familiar and unfamiliar individuals in the lizard Liolaemus tenuis (Liolaemidae), a species in which males are territorial. The behaviours recorded were attack, warning, evasion, and submission, and the latencies to the first aggressive (attack or warning) behaviour. Additionally, we assessed the ability of individuals to remember a familiar conspecific after a period without social interaction. Individual males reduced and delayed aggressive behaviour directed towards socially familiar individuals compared with unfamiliar ones. These results suggest that males distinguished between familiar and unfamiliar conspecific males and are in agreement with the ‘dear enemy’ phenomenon. Other behaviours were similar in the contests between familiar and unfamiliar individuals. Recognition of familiar conspecifics was lost after 20 d without social interactions. This may be relevant for interactions with floater males or with neighbours that lose their territory and subsequently attempt to fight for their ex‐neighbour's territory.     

Conspecific and heterospecific information use in bumblebees

Heterospecific social learning has been understudied in comparison to interactions between members of the same species. However, the learning mechanisms behind such information use can allow animals to be flexible in the cues that are used. This raises the question of whether conspecific cues are inherently more influential than cues provided by heterospecifics, or whether animals can simply use any cue that predicts fitness enhancing conditions, including those provided by heterospecifics. To determine how freely social information travels across species boundaries, we trained bumblebees (Bombus terrestris) to learn to use cues provided by conspecifics and heterospecific honey bees (Apis mellifera) to locate valuable floral resources. We found that heterospecific demonstrators did not differ from conspecifics in the extent to which they guided observers'' choices, whereas various types of inorganic visual cues were consistently less effective than conspecifics. This was also true in a transfer test where bees were confronted with a novel flower type. However, in the transfer test, conspecifics were slightly more effective than heterospecific demonstrators. We then repeated the experiment with entirely naïve bees that had never foraged alongside conspecifics before. In this case, heterospecific demonstrators were equally efficient as conspecifics both in the initial learning task and the transfer test. Our findings demonstrate that social learning is not a unique process limited to conspecifics and that through associative learning, interspecifically sourced information can be just as valuable as that provided by conspecific individuals. Furthermore the results of this study highlight potential implications for understanding competition within natural pollinator communities.     

Spatial patterns of the frog Oophaga pumilio in a plantation system are consistent with conspecific attraction

The conspecific attraction hypothesis predicts that individuals are attracted to conspecifics because conspecifics may be cues to quality habitat and/or colonists may benefit from living in aggregations. Poison frogs (Dendrobatidae) are aposematic, territorial, and visually oriented—three characteristics which make dendrobatids an appropriate model to test for conspecific attraction. In this study, we tested this hypothesis using an extensive mark‐recapture dataset of the strawberry poison frog (Oophaga pumilio) from La Selva Biological Station, Costa Rica. Data were collected from replicate populations in a relatively homogenous Theobroma cacao plantation, which provided a unique opportunity to test how conspecifics influence the spatial ecology of migrants in a controlled habitat with homogenous structure. We predicted that (1) individuals entering a population would aggregate with resident adults, (2) migrants would share sites with residents at a greater frequency than expected by chance, and (3) migrant home ranges would have shorter nearest‐neighbor distances (NND) to residents than expected by chance. The results were consistent with these three predictions: Relative to random simulations, we observed significant aggregation, home‐range overlap, and NND distribution functions in four, five, and six, respectively, of the six migrant–resident groups analyzed. Conspecific attraction may benefit migrant O. pumilio by providing cues to suitable home sites and/or increasing the potential for social interactions with conspecifics; if true, these benefits should outweigh the negative effects of other factors associated with aggregation. The observed aggregation between migrant and resident O. pumilio is consistent with conspecific attraction in dendrobatid frogs, and our study provides rare support from a field setting that conspecific attraction may be a relevant mechanism for models of anuran spatial ecology.     

Implications of conspecific background noise for features of blue tit, Cyanistes caeruleus , communication networks at dawn

Communication among animals often comprises several signallers and receivers within the signal’s transmission range. In such communication networks, individuals can extract information about differences in relative performance of conspecifics by eavesdropping on their signalling interactions. In songbirds, information can be encoded in the timing of signals, which either alternate or overlap, and both male and female receivers may utilise this information when engaging in territorial interactions or making reproductive decisions, respectively. We investigated how conspecific background noise at dawn may overlay and possibly constrain the perception of such singing patterns. We simulated a small communication network of blue tits, Cyanistes caeruleus, at dawn in spring. Two loudspeakers simulated a singing interaction which was recorded from four different receiver positions simulating potential eavesdroppers. During the recordings, resident blue tit males were vocalising and created natural conspecific background noise. Levels of conspecific background noise were high and varied among positions of potential eavesdroppers. We conclude that conspecific background vocalisations may potentially constrain the perception of singing patterns and may constitute costs for eavesdroppers. On the other hand, signallers may position themselves strategically and privatise their interactions.     

Salient eyes deter conspecific nest intruders in wild jackdaws (Corvus monedula)

Animals often respond fearfully when encountering eyes or eye-like shapes. Although gaze aversion has been documented in mammals when avoiding group-member conflict, the importance of eye coloration during interactions between conspecifics has yet to be examined in non-primate species. Jackdaws (Corvus monedula) have near-white irides, which are conspicuous against their dark feathers and visible when seen from outside the cavities where they nest. Because jackdaws compete for nest sites, their conspicuous eyes may act as a warning signal to indicate that a nest is occupied and deter intrusions by conspecifics. We tested whether jackdaws’ pale irides serve as a deterrent to prospecting conspecifics by comparing prospectors’ behaviour towards nest-boxes displaying images with bright eyes (BEs) only, a jackdaw face with natural BEs, or a jackdaw face with dark eyes. The jackdaw face with BEs was most effective in deterring birds from making contact with nest-boxes, whereas both BE conditions reduced the amount of time jackdaws spent in proximity to the image. We suggest BEs in jackdaws may function to prevent conspecific competitors from approaching occupied nest sites.     

Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans

The pintado (Pseudoplatystoma coruscans) is a ferocious carnivorous catfish with evident cannibalistic behaviour; its nocturnal habits are related to its ability to use predominately chemical sensorial modalities. This study investigated whether the pintado distinguishes conspecifics of different body sizes using chemical cues, which may reflect different physiological conditions such as hunger or stress. Pintados were observed when receiving water conditioned by either larger or similar-size conspecifics. A control group consisted of pintados receiving unconditioned water. Twelve repetitions were used for each condition. Feeding-like behaviours were investigated in the receiver fish and showed that they responded only to the conditioned water. Furthermore, a higher frequency of responses occurred when the water was conditioned by a similar-size conspecific. Thus, it is concluded that pintados are able to recognize conspecific size by chemical cues related to size and that this ability contributes to the individual's decision making on whether to approach or to avoid the conspecific.     

Impaired social contacts with familiar anesthetized conspecific in CA3‐restricted brain‐derived neurotrophic factor knockout mice

Familiarity is conveyed by social cues and determines behaviors toward conspecifics. Here, we characterize a novel assay for social behaviors in mice—contacts with anesthetized conspecific—which eliminates reciprocal interactions, including intermale aggression and shows behaviors that are independent of the demonstrator's activity. During the initial 10 minutes (phase‐1), the wild‐type (WT) subjects contacted the anesthetized conspecifics vigorously regardless of familiarity. During the subsequent 80 minutes (phase‐2), however, they contacted more with familiar than unfamiliar conspecifics. We then applied this test to highly aggressive mice with a hippocampal CA3‐restricted knockout (KO) of brain‐derived neurotrophic factor (BDNF), in which aggression may mask other social behaviors. The KO mice showed less preference for contacting familiar conspecifics than did WT mice during phase‐2 but no differences during phase‐1. Among nonsocial behaviors, WT mice also spent less time eating in the presence of familiar than with unfamiliar conspecifics, which was not seen in KO mice. In addition, KO mice exhibited reduced pain sensitization. Altogether, these findings suggest that CA3‐specific deletion of BDNF results in deficits in circuits that process social cues from familiar conspecifics as well as pain and may underlie empathy‐like behaviors.     

The effects of cross-fostering on the behaviour of two species of North American lemmings, dicrostonyx groenlandicus and lemmus trimucronatus: II. Sexual behaviour

The role of the maternal environment in development of sexual behaviour was investigated by reciprocally cross-fostering two species of lemmings (Dicrostonyx groenlandicus and Lemmus trimucronatus). Non-fostered and within-species-fostered animals served as controls. When adult, cross-fostered (CF) animals engaged in more contact social and sexual behaviours with the foster species than did controls. Lemmings reared by conspecific dams directed sexual behaviour exclusively toward conspecifics. Since CF animals also mated with conspecifics, cross-fostering appears to have resulted in a broadening of ‘species identity’ to include the foster species. These results suggest that neonatal learning of the species characteristics of the mother is important in the ontogeny of premating sexual isolation in these species.     

Visual co-orientation and expectations about attentional orientation in pileated gibbons (Hylobates pileatus)

This study investigated attentional processes in a sample of captive gibbons. An initial aim of the research was to examine subjects' ability to co-orient with photographic images of both conspecific and human models. The gibbons' expectancies about the focus of another's attention was then also assessed, with an expectancy violation paradigm revealing subjects' sensitivity to an incompatibility between visual orientation and the position of a target object. The gibbons were exposed to two conditions; consistent sequences in which the stimulus individual directed attention towards a target object, and inconsistent sequences in which the model's attentional focus was incompatible with the location of this article. Analyses of the subjects' responses were made according to the direction of gazes and the time spent inspecting the depicted model in each of these conditions. The results reveal a tendency for visual co-orientation with both conspecific and human models, suggesting that gibbons are competent in detecting the visual orientation of other species as well as their own. Furthermore, the subjects' tendency to look longer and check back to the depicted model in response to violations in the relationship between an agent and object (target appearing in an opposite direction to model's gaze), suggests that they possess some knowledge of how visual gaze direction relates to external stimuli.     

Tolerance and Social Facilitation in the Foraging Behaviour of Free‐Ranging Crows (Corvus corone corone; C. c. cornix)

Social foraging provides animals with opportunities to gain knowledge about available food. Studies indicate that animals are influenced by social context during exploration and are able to learn socially. Carrion and hooded crows, which are opportunistic generalists with flexible social systems, have so far received little focus in this area. We combined observational and experimental approaches to investigate social interactions during foraging and social influences on crow behaviour within a free‐ranging population at Vienna Zoo, which included 115 individually marked crows. We expected the crows to be tolerant of conspecifics during foraging due to high food abundance. We predicted that social context would enhance familiar object exploration, as well as a specific foraging strategy: predation by crows on other species. We found that crows were highly tolerant of one another, as reflected by their high rates of cofeeding – where they fed directly beside conspecific(s) – relative to affiliative or agonistic interactions. Evidence for social facilitation – when the observer's behaviour is affected by the mere presence of a model – was found in both object exploration and predation behaviour. Specifically, crows touched the objects more frequently when others were present (whilst only approaching the objects when alone), and conspecifics were present more frequently during predation events involving the high‐risk target species. Evidence for enhancement during object exploration – where the observer's attention is drawn to a place or object by a model's actions – was not confirmed in this context. Our results highlight the role played by the presence of conspecifics across different contexts: natural foraging behaviour, familiar object exploration and a specific foraging strategy. To our knowledge, this is one of the first corvid studies aimed at teasing apart specific social influence and learning mechanisms in the field. These crows therefore make promising candidates for studying social learning and its consequences under naturalistic conditions.     

Conspecifics as informers and competitors: an experimental study in foraging bumble-bees

Conspecifics are usually considered competitors negatively affecting food intake rates. However, their presence can also inform about resource quality by providing inadvertent social information. Few studies have investigated whether foragers perceive conspecifics as informers or competitors. Here, we experimentally tested whether variation in the density of demonstrators ('none', 'low' and 'high'), whose location indicated flower profitability, affected decision-making of bumble-bees Bombus terrestris. Bumble-bees foraged on either 'simple' (two colours) or 'complex' (four colours) artificial floral communities. We found that conspecifics at low density may be used as sources of information in first flower choices, whereas they appeared as competitors over the whole foraging sequence. Low conspecific densities improved foragers' first-visit success rate in the simple environment, and decreased time to first landing, especially in the complex environment. High conspecific densities did not affect these behavioural parameters, but reduced flower constancy in both floral communities, which may alter the efficiency of pollinating visits. These results suggest that the balance of the costs and benefits of conspecific presence varies with foraging experience, floral community and density. Spatio-temporal scales could thus be an important determinant of social information use. This behavioural flexibility should allow bumble-bees to better exploit their environment.     

Indirect Information Transfer: Three‐Spined Sticklebacks Use Visual Alarm Cues From Frightened Conspecifics About an Unseen Predator

Animals can attempt to reduce uncertainty about their environment by gathering information personally or by observing others' interactions with the environment. There are several sensory modalities that can be used to transmit social information from chemical to visual to audible cues. When predation risk is variable, visual cues of conspecific behavior might be especially telling about the presence of a potential threat; however, most studies couple visual and chemical cues together. Here, we tested whether visual behavioral cues from frightened conspecifics were sufficient to indirectly transfer information about the presence of an unseen predator in three‐spined sticklebacks. Our results demonstrate that visual behavioral cues from conspecifics about the presence of a predator are sufficient to induce an antipredator response. This suggests that information transfer can occur rapidly in the absence of chemical cues and that some individuals weigh social information more heavily than others.     

Anemonefishes rely on visual and chemical cues to correctly identify conspecifics

Organisms rely on sensory cues to interpret their environment and make important life-history decisions. Accurate recognition is of particular importance in diverse reef environments. Most evidence on the use of sensory cues focuses on those used in predator avoidance or habitat recognition, with little information on their role in conspecific recognition. Yet conspecific recognition is essential for life-history decisions including settlement, mate choice, and dominance interactions. Using a sensory manipulated tank and a two-chamber choice flume, anemonefish conspecific response was measured in the presence and absence of chemical and/or visual cues. Experiments were then repeated in the presence or absence of two heterospecific species to evaluate whether a heterospecific fish altered the conspecific response. Anemonefishes responded to both the visual and chemical cues of conspecifics, but relied on the combination of the two cues to recognize conspecifics inside the sensory manipulated tank. These results contrast previous studies focusing on predator detection where anemonefishes were found to compensate for the loss of one sensory cue (chemical) by utilizing a second cue (visual). This lack of sensory compensation may impact the ability of anemonefishes to acclimate to changing reef environments in the future.

     

Avoid your neighbours: size-determined spatial distribution patterns among northern pike individuals

The spatial distribution of individual animals may both cause and be caused by intra- and/or interspecific interactions. This work aims primarily on effects of intraspecific interactions. Agonistic and unequally strong interactions among conspecifics should make the within-population distribution of individuals to be characterised by spatial avoidance of potentially risky conspecifics, according to the individual risks perceived. This process should affect individual performance and involve individual tradeoffs, as failing to adequately avoid risky conspecifics could incur unnecessary costs, while, at the same time, successful conspecific avoidance may reduce access to patches favourable for e.g. foraging or sheltering. Intraspecific agonistic behaviours, such as cannibalism and competition, are likely to have prominent effects in size-structured populations. It is therefore reasonable to assume spatial avoidance of intraspecific risks according to individuals' size relationships in such populations. With this field investigation I show that individuals of northern pike spatially avoid larger conspecifics. This avoidance creates a size-influenced and spatially clumped distribution pattern among pike individuals. At low pike densities, however, distances between individuals increase, allowing for an even distribution pattern to appear. The spatial distribution patterns among piscivore individuals should affect both the individual performance of predators and the potential for spatial anti-predatory responses of their prey, and hence be a factor in consumer–resource interactions.     

Reproductive character displacement generates reproductive isolation among conspecific populations: an artificial neural network study

When interactions with heterospecifics prevent females from identifying conspecific mates, natural selection can promote the evolution of mating behaviours that minimize such interactions. Consequently, mating behaviours may diverge among conspecific populations in sympatry and in allopatry with heterospecifics. This divergence in conspecific mating behaviours-reproductive character displacement-can initiate speciation if mating behaviours become so divergent as to generate reproductive isolation between sympatric and allopatric conspecifics. We tested these ideas by using artificial neural networks to simulate the evolution of conspecific mate recognition in populations sympatric and allopatric with different heterospecifics. We found that advertisement calls diverged among the different conspecific populations. Consequently, networks strongly preferred calls from their own population to those from foreign conspecific populations. Thus, reproductive character displacement may promote reproductive isolation and, ultimately, speciation among conspecific populations.