Are conspecific social videos rewarding to chimpanzees (Pan troglodytes)? A test of the social motivation theory

Many claim that social stimuli are rewarding to primates, but few, if any, studies have explicitly demonstrated their reward value. Here, we examined whether chimpanzees would produce overt responses for the opportunity to view conspecific social, compared to dynamic (video: Experiment 1) and static (picture: Experiment 2) control content. We also explored the relationships between variation in social reward and social behavior and cognition. We provided captive chimpanzees with access to a touchscreen during four, one-hour sessions (two ‘conspecific social’ and two ‘control’). The sessions consisted of ten, 15-second videos (or pictures in Experiment 2) of either chimpanzees engaging in a variety of behaviors (social condition) or vehicles, humans, or other animals engaged in some activity (control condition). For each chimpanzee, we recorded the number of responses to the touchscreen and the frequency of watching the stimuli. Independent t-tests revealed no sex or rearing differences in touching and watching the social or control videos (p>0.05). Repeated measures ANOVAs showed chimpanzees touched and watched the screen significantly more often during the social compared to control video sessions. Furthermore, although chimpanzees did not touch the screen more often during social than control picture sessions in Experiment 2, they did watch the screen more often. Additionally, chimpanzees that previously performed better on a task of social cognition and engaged in more affiliative behavior watched a higher percentage of social videos during the touchscreen task. These results are consistent with the social motivation theory, and indicate social stimuli are intrinsically rewarding, as chimpanzees made more overt responses for the opportunity to view conspecific social, compared to control, content.

Agonism and grooming behavior explain social status effects on physiology and gene regulation in rhesus macaques

Variation in social status predicts molecular, physiological, and life history outcomes across a broad range of species, including our own. Experimental studies indicate that some of these relationships persist even when the physical environment is held constant. Here, we draw on data sets from one such study-experimental manipulation of dominance rank in captive female rhesus macaques-to investigate how social status shapes the lived experience of these animals to alter gene regulation, glucocorticoid physiology, and mitochondrial DNA phenotypes. We focus specifically on dominance rank-associated dimensions of the social environment, including both competitive and affiliative interactions. Our results show that simple summaries of rank-associated behavioral interactions are often better predictors of molecular and physiological outcomes than dominance rank itself. However, while measures of immune function are best explained by agonism rates, glucocorticoid-related phenotypes tend to be more closely linked to affiliative behavior. We conclude that dominance rank serves as a useful summary for investigating social environmental effects on downstream outcomes. Nevertheless, the behavioral interactions that define an individual's daily experiences reveal the proximate drivers of social status-related differences, and are especially relevant for understanding why individuals who share the same social status sometimes appear physiologically distinct.

DNA Damage as a Potential Non-Invasive Indicator of Welfare: A Preliminary Study in Zoo-Housed Grizzly Bears (Ursus arctos horribilis)

Measures of oxidative stress have potential for integrating positive and negative life experiences into comprehensive cellular indicators of animal welfare. We explored this possibility when three adult grizzly bear brothers at the Detroit Zoo were temporarily moved to a smaller habitat while their primary home was expanded. We expected that the spatial compression and construction activity might be sources of stress. We observed increased social play and other affiliative behavior in the smaller habitat, and we used daily fecal samples (17 to 24 per bear) to examine whether concentrations of fecal glucocorticoid metabolites (FGM) and 8-hydroxy-2′-deoxyguanosine (8-OHdG, a by-product of DNA damage) were correlated with social behavior. Our overall aim was to explore 8-OHdG as a potential indicator of welfare based on the prediction that 8-OHdG would be lower when more positive social interactions occurred. Concentrations of fecal 8-OHdG increased significantly with higher FGM concentrations, supporting a potential relationship between adrenal activity and rates of DNA damage. However, we found that on days when they engaged in higher rates of affiliative interactions, there were trends for 8-OHdG concentrations to increase for one bear and decrease for another, and no relationship for the third bear. These preliminary results should be interpreted with caution, but suggest a potential relationship between social behavior and 8-OHdG that is modulated by health, personality, or other individual factors. Further validation research is needed, but 8-OHdG may have promise as a non-invasive, cumulative indicator of animal welfare.

Intranasal oxytocin reduces pre-courtship aggression and increases paternal response in California mice (Peromyscus californicus)

Oxytocin (OXT) is a neuropeptide that can facilitate prosocial behavior and decrease social stress and anxiety. We investigated whether acute pulses of intranasal (IN) OXT influenced social behavior during social challenges that are likely to occur throughout the lifespan of a wild mouse. To test this, we examined the acute effects of IN OXT in the male California mouse (Peromyscus californicus), a monogamous, biparental, and territorial rodent, using a within-subjects longitudinal design. Social challenges included a pre-courtship male-female encounter conducted during the initial aggressive and not the following affiliative phase of courtship, same-sex resident intruder test, and parental care test, with each test and dose separated by at least two weeks. Males were treated with intranasal infusions of 0.8 IU/kg OXT or saline controls 5-min before each behavioral test, receiving a total of three treatments of either IN OXT or saline control. We predicted that IN OXT would 1) decrease aggression and increase affiliation during the pre-courtship aggression phase, 2) increase aggression during resident intruder paradigms and 3) increase paternal care and vocalizations during a paternal care test. As predicted, during pre-courtship aggression with a novel female, IN OXT males displayed less contact aggression than control males, although with no change in affiliative behavior. However, post-pairing, during the resident intruder test, IN OXT males did not differ from control males in contact aggression. During the paternal care test, IN OXT males were quicker to approach their pups than control males but did not differ in vocalizations produced, unlike our previous research demonstrating an effect on vocalizations in females. In summary, during pre-courtship aggression and the paternal care test, IN OXT promoted prosocial approach; however, during the resident intruder test IN OXT did not alter social approach. These data suggest that IN OXT promotes prosocial approach specifically in social contexts that can lead to affiliation.

The role of state feelings of loneliness in the situational regulation of social affiliative behavior: Exploring the regulatory relations within a multilevel framework

Previous empirical evidence suggests that the engagement in social interactions across different everyday contexts occurs in a manner highly responsive to a person’s social affiliation needs. As has been shown repeatedly, social engagement (as well as disengagement) can be predicted from earlier situational need states, implying that homeostatic principles underlie a person’s social affiliative behaviors. However, little is known about the role of emotion in these regulative processes. For this reason, the present exploratory study investigated the predictive role of state feelings of loneliness in subsequent engagement in social interaction. Since loneliness is conceptually associated with both the need to reaffiliate as well as self-protecting tendencies potentially hindering engagement in social contact, the study investigated the possibility of both increases and decreases in social contacts resulting from state feelings of loneliness. Adopting an experience sampling methodology (ESM), a sample of 65 participants was recruited from a local university and was followed for 14 days. Subjects were prompted several times a day to rate their feeling states and the quantity of social interactions, using a fixed interval assessment schedule. Statistical analyses using multilevel analysis indicated that state feelings of loneliness had complex quadratic effects upon subsequent social interaction, leading to both increases and decreases in subsequent social interaction. Moreover, these effects were contingent upon previous engagement in social interaction, implying spillover effects across social contexts that are conditionally mediated by feelings of loneliness. These findings clearly imply an important, albeit complex role of state feelings of loneliness in the regulation of social affiliation, both as a predictor and a consequence of social interaction. These exploratory findings are discussed against the background of methodological and conceptual limitations, and several recommendations for future studies are made.

Wild geladas (Theropithecus gelada) in crops—more than in pasture areas—reduce aggression and affiliation

Human–primate interfaces are expanding and, despite recent studies on primates from peri-urban environments, little research exists on the impact of agriculture and/or pasture areas on primate social behavior and health. We assessed how crop/pasture areas potentially alter social behavior and health of wild geladas (Theropithecus gelada) frequenting the unprotected area of Kundi (Ethiopia). We predicted that compared to pasture areas, crop areas (i) would be more challenging for geladas (prediction 1) and (ii) would have a greater impact on both aggressive and affiliative behavior, by reducing grooming time and enhancing competition (prediction 2). During January–May 2019 and December 2019–February 2020, we collected data (via scan, focal animal sampling, and video analyses) on direct human disturbance, external signs of pathologies and social behavior of 140 individuals from 14 one-male units and two all-male units. Animals experienced the highest level of human disturbance in crop areas (in line with prediction 1). Individuals from the groups preferentially frequenting crop areas showed the highest prevalence of external signs of pathologies consistent with chemical and biological contamination (alopecia/abnormally swollen parts). We collected 48 fecal samples. Samples from frequent crop users contained the highest rates of parasitic elements/gram (egg/larva/oocyst/cyst) from Entamoeba histolytica/dispar, a parasite common in human settlements of the Amhara region. In crop areas, subjects spent less time grooming but engaged in lower rates of intense aggression (in partial agreement with prediction 2). We speculate that the reduction in social behavior may be a tactic adopted by geladas to minimize the likelihood of detection and maximize food intake while foraging in crops.

Cardiovascular Neuroendocrinology: Emerging Role for Neurohypophyseal Hormones in Pathophysiology

Arginine vasopressin (AVP) and oxytocin (OXY) are released by magnocellular neurosecretory cells that project to the posterior pituitary. While AVP and OXY currently receive more attention for their contributions to affiliative behavior, this mini-review discusses their roles in cardiovascular function broadly defined to include indirect effects that influence cardiovascular function. The traditional view is that neither AVP nor OXY contributes to basal cardiovascular function, although some recent studies suggest that this position might be re-evaluated. More evidence indicates that adaptations and neuroplasticity of AVP and OXY neurons contribute to cardiovascular pathophysiology.

Post-weaning stroking stimuli induce affiliative behavior toward humans and influence brain activity in female rats

Gentle touch contributes to affiliative interactions. We investigated the effects of gentle stroking in female rats on the development of affiliative behaviors toward humans and we exploratively examined brain regions in which activity was influenced by stroking. Rats that had received stroking stimuli repeatedly after weaning emitted 50-kHz calls, an index of positive emotion, and showed affiliative behaviors toward the experimenter. Hypothalamic paraventricular oxytocin neurons were activated in the rats after stroking. The septohypothalamic nucleus (SHy) in the post-weaningly stroked rats showed decreased activity in response to stroking stimuli compared with that in the non-stroked control group. There were negative correlations of neural activity in hypothalamic regions including the SHy with the number of 50-kHz calls. These findings revealed that post-weaning stroking induces an affiliative relationship between female rats and humans, possibly via activation of oxytocin neurons and suppression of the activity of hypothalamic neurons.