Social buffering of the stress response: insights from fishes

Social buffering of stress refers to the effect of a social partner in reducing the cortisol or corticosterone response to a stressor. It has been well studied in mammals, particularly those that form pair bonds. Recent studies on fishes suggest that social buffering of stress also occurs in solitary species, gregarious species that form loose aggregations and species with well-defined social structures and bonds. The diversity of social contexts in which stress buffering has been observed in fishes holds promise to shed light on the evolution of this phenomenon among vertebrates. Equally, the relative simplicity of the fish brain is advantageous for identifying the neural mechanisms responsible for social buffering. In particular, fishes have a relatively small and simple forebrain but the brain regions that are key to social buffering, including the social behaviour network, the amygdala and the hypothalamic–pituitary–adrenal/interrenal axis, are functionally conserved across vertebrates. Thus, we suggest that insight into the mechanistic and evolutionary underpinnings of stress buffering in vertebrates can be gained from the study of social buffering of stress in fishes.     

Social modulation of fear: Facilitation vs buffering

Social behaviors largely constitute mutual exchanges of social cues and the responses to them. The adaptive response also requires proper interpretation of the current context. In fear behaviors, social signals have bidirectional effects—some cues elicit or enhance fear whereas other suppress or buffer it. Studies on the social facilitation and social buffering of fear provide evidence of competition between social cues of opposing meanings. Co‐expression of opposing cues by the same animal may explain the contradicting outcomes from the interaction between naive and frightened conspecifics, which reflect the fine balance between fear facilitation and buffering. The neuronal mechanisms that determine that balance provide an exciting target for future studies to probe the brain circuits underlying social modulation of emotional behaviors.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.     

Theories and possible processes of action in animal assisted interventions

Different positive effects of interactions with animals, such as reduction of stress reactions, depressive mood, anxiety, aggression, and pain, and promotion of trust, calmness, motivation, and concentration have been documented by research on human–animal interaction (HAI), including animal assisted interventions (AAIs). Potential biological, psychological, and social processes may underpin these effects. Theories of why this may occur include biophilia, anthropomorphism, a focus on the experiential system instead of the verbal-symbolic system, motivation, activation of the oxytocin system, attachment and caregiving including provision of social support for stress buffering, and distraction processes. Understanding how animals may positively affect educational and therapeutic settings, in particular for individuals with psychical and psychosocial challenges, and finding what special indications for AAI exist, and which preconditions of learning in the client or the setting could potentially be enhanced, might provide not only a better rationale for AAIs but also promote their efficacy.     

Salubrious effects of oxytocin on social stress-induced deficits

Social relationships are a fundamental aspect of life, affecting social, psychological, physiological, and behavioral functions. While positive social interactions can attenuate stress and promote health, the social environment can also be a major source of stress when it includes social disruption, confrontation, isolation, or neglect. Social stress can impair the basal function and stress-induced activation of the hypothalamic-pituitary-adrenal (HPA) axis, impairing function of multiple biological systems and posing a risk to mental and physical health. In contrast, social support can ameliorate stress-induced physiological and immunological deficits, reducing the risk of subsequent psychological distress and improving an individual's overall well-being. For better clinical treatment of these physiological and mental pathologies, it is necessary to understand the regulatory mechanisms of stress-induced pathologies as well as determine the underlying biological mechanisms that regulate social buffering of the stress system. A number of ethologically relevant animal models of social stress and species that form strong adult social bonds have been utilized to study the etiology, treatment, and prevention of stress-related disorders. While undoubtedly a number of biological pathways contribute to the social buffering of the stress response, the convergence of evidence denotes the regulatory effects of oxytocin in facilitating social bond-promoting behaviors and their effect on the stress response. Thus, oxytocin may be perceived as a common regulatory element of the social environment, stress response, and stress-induced risks on mental and physical health. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Friends with benefits: Social support and its relevance for farm animal welfare

Despite growing interest in promoting positive welfare, rather than just alleviating poor welfare, potential measures of good welfare, and means to provide it, have remained elusive. In humans social support improves stress-coping abilities, health, and promotes positive psychological welfare. Therefore, social support may be a key approach to promote positive physical and psychological welfare in farm animals. However, the roles of positive social behaviors and social support have been overlooked in comparison to negative social behaviors such as agonistic interactions. The benefits of social partners on an animal's stress coping abilities and welfare are yet poorly understood.The purpose of this paper is to review the protective or buffering effects of social support against stressful challenges and its potential implications for farm animal welfare. The biology of social support is first presented with its behavior, endocrine, autonomic and immune components. The major factors modulating the social support process are then synthesized. Research and implications for animal welfare in different farm species are discussed. Lastly, this review identifies research areas that especially deserve further attention in our effort to understand and implement social support in farm animal welfare.Social support could constitute one of the foundations for welfare researchers to leap from the absence of negative welfare to the provision of positive welfare and emotional experiences.     

Stressful life events, social support networks, and the physical and mental health of urban black adults

The direct and the buffering effects of social support networks have been documented, but few studies have examined their health outcomes for blacks and, specifically, the differences in physical and mental health. This study uses six measures of social support to examine the relationships of social support to health outcomes for black males and females. The data are from a community sample of 451 urban black adults. Results show significant differences by sex according to source of social support and particular health outcomes. Number of nearby relatives and perceived social support have direct and buffering effects, respectively, on mental health for black females, but no significant influences emerge for black males. On the other hand, the number of confidants for black males and the degree of religiosity among black females were inversely related to physical health, suggesting differences in conceptual models of social support for mental and physical health.     

Social Contact Following Severe Aggression in Rhesus Macaques (Macaca mulatta): A New Test of the Consolation Hypothesis

Previous studies on macaque species revealed no evidence of consolation: affiliative contact between the loser of an aggressive interaction and a third party. However, typically, the researchers used short observation periods and latency to make first affiliative contact as a dependent measure. Based on social stress buffering literature, I predicted that by employing longer observation periods and percentage of time in affiliative contact as a dependent measure, I would be more likely to detect increases in affiliative contact following aggression. I observed adult female rhesus macaques for 1 hr after they received severe aggression and for 1 hr after some affiliative contact, and measured time spent in affiliative contact using instantaneous recording at 30-sec intervals. Contrary to prediction, victims of attack did not spend a greater percentage of time in affiliative contact postaggression as compared to postaffiliation. Subjects were also less likely to initiate contact with other individuals and were more likely to have contact with individuals that were dominant to their aggressor, following aggression. These results provide converging evidence that affiliative contact is not increased following aggression in macaques. I discuss the failure to bear out the predictions based on the social stress buffering literature in terms of rhesus social dynamics, the nature of aggression as a stressor, and possible mechanisms for the social stress buffering effect.     

Reproductive conflict delays the recovery of an endangered social species

1. Evolutionary theory predicts that individuals, in order to increase their relative fitness, can evolve behaviours that are detrimental for the group or population. This mismatch is particularly visible in social organisms. Despite its potential to affect the population dynamics of social animals, this principle has not yet been applied to real-life conservation. 2. Social group structure has been argued to stabilize population dynamics due to the buffering effects of nonreproducing subordinates. However, competition for breeding positions in such species can also interfere with the reproduction of breeding pairs. 3. Seychelles magpie robins, Copsychus sechellarum, live in social groups where subordinate individuals do not breed. Analysis of long-term individual-based data and short-term behavioural observations show that subordinates increase the territorial takeover frequency of established breeders. Such takeovers delay offspring production and decrease territory productivity. 4. Individual-based simulations of the Seychelles magpie robin population parameterized with the long-term data show that this process has significantly postponed the recovery of the species from the Critically Endangered status. 5. Social conflict thus can extend the period of high extinction risk, which we show to have population consequences that should be taken into account in management programmes. This is the first quantitative assessment of the effects of social conflict on conservation.     

The integration of dominance and social bonding in primates

Social dominance is usually viewed from the perspective of intragroup competition over access to limited resources. The present paper, while not denying the importance of such competition, discusses the dominance concept among monkeys and apes in the context of affiliative bonding, social tolerance, and the reconciliation of aggressive conflicts. Two basic proximate mechanisms are supposed to provide a link between dominance and interindividual affiliation, namely, formalization of the dominance relationship (i.e., unequivocal communication of status), and conditional reassurance (i.e., the linkage of friendly coexistence to formalization of the relationship). Ritualized submission is imposed upon losers of dominance struggles by winners; losers are offered a "choice" between continued hostility or a tolerant relationship with a clearly signalled difference in status. If these two social mechanisms are lacking, aggression is bound to have dispersive effects. In their presence, aggression becomes a well-integrated, even constructive component of social life. In some higher primates this process of integration has reached the stage where status differences are strongly attenuated. In these species, sharing and trading can take the place of overt competition. The views underlying this "reconciled hierarchy" model are only partly new, as is evident from a review of the ethological literature. Many points are illustrated with data on a large semi-captive colony of chimpanzees (Pan troglodytes), particularly data related to striving for status, reconciliation behavior, and general association patterns. These observations demonstrate that relationships among adult male chimpanzees cannot be described in terms of a dichotomy between affiliative and antagonistic tendencies. Male bonding in this species has not been achieved by an elimination of aggression, but by a set of powerful buffering mechanisms that mitigate its effects. Although female chimpanzees do exhibit a potential for bonding under noncompetitive conditions, they appear to lack the buffering mechanisms of the males.     

The strain of an accompanying conspecific affects the efficacy of social buffering in male rats

Social buffering is a phenomenon in which stress in an animal is ameliorated when the subject is accompanied by a conspecific animal(s) during exposure to distressing stimuli. We previously reported that in male Wistar rats, the presence of another Wistar rat mitigates conditioned fear responses to an auditory conditioned stimulus (CS). Subsequent analyses revealed several characteristics of this social buffering of conditioned fear responses. However, information regarding the specificity of accompanying conspecifics is still limited. In the present study, we assessed whether rats of other strains could induce social buffering in Wistar rats. When a fear-conditioned Wistar subject was re-exposed to the CS alone, we observed increased freezing and decreased investigation and walking, as well as elevated corticosterone levels. The presence of a Wistar, Sprague–Dawley, or Long–Evans rat blocked these responses, suggesting that social buffering was induced by these strains of rats. In contrast, a Fischer 344 rat did not induce social buffering in the Wistar subject. We further found that an inbred Lewis rat induced social buffering whereas a Brown Norway rat, a strain that has been established independently from Wistar rats, did not. These results suggest that the difference in origin, rather than the inbred or outbred status of the associate rat, seemed to account for the lack of social buffering induced by the F344 rats. Based on these findings, we conclude that strains of an accompanying conspecific can affect the efficacy of social buffering in rats.     

Kin investment in wage-labor economies

Various human groups, from food foragers to inner-city urban Americans, have used widespread sharing of resources through kin networks as a means of buffering themselves against fluctuations in resource availability in their environments. This paper addresses the effects of progressive incorporation into a wage-labor economy on the benefits of traditional kin networks for two social classes in urban South India. Predictions regarding the effects of kin network wealth, education, and size on child and spouse characteristics and methods of financing marriages are tested using various regression techniques. Despite the rapid growth of participation in a wage-labor economy, it is found that kin network characteristics still have an important impact on investment behavior among families in Bangalore in both social classes. Network wealth is found to have a positive effect on child and spouse characteristics, and large networks are found to act as significant drains on family resources. However, the results for education are broadly consistent with an interpretation of increasing family autonomy as parents’ education has a far stronger influence on child and spouse characteristics across categories than network education does. Finally, professional-class parents are found to prefer financing marriages using formal mechanisms such as savings and bank loans while working-class parents preferentially finance marriages using credit from relatives and friends.     

Social buffering ameliorates conditioned fear responses in female rats

The stress experienced by an animal is ameliorated when the animal is exposed to distressing stimuli along with a conspecific animal(s). This is known as social buffering. Previously, we found that the presence of an unfamiliar male rat induced social buffering and ameliorated conditioned fear responses of a male rat subjected to an auditory conditioned stimulus (CS). However, because our knowledge of social buffering is highly biased towards findings in male subjects, analyses using female subjects are crucial for comprehensively understanding the social buffering phenomenon. In the present studies, we assessed social buffering of conditioned fear responses in female rats. We found that the estrus cycle did not affect the intensity of the rats' fear responses to the CS or their degree of vigilance due to the presence of a conspecific animal. Based on these findings, we then assessed whether social buffering ameliorated conditioned fear responses in female rats without taking into account their estrus cycles. When fear conditioned female rats were exposed to the CS without the presence of a conspecific, they exhibited behavioral responses, including freezing, and elevated corticosterone levels. By contrast, the presence of an unfamiliar female rat suppressed these responses. Based on these findings, we conclude that social buffering can ameliorate conditioned fear responses in female rats.     

Social relationship and hair cortisol level in captive male chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Understanding how social relationships affect long-term stress is important because stress has a profound impact on the welfare of animals and social relationships often exert a strong influence on their stress responses. The purpose of this study was to investigate the relationship between social behaviors and long-term stress levels as assessed by hair cortisol (HC) concentration. The subjects were 11 chimpanzees living in an all-male group (divided into two sub-groups) in Kumamoto Sanctuary, Kyoto University, Japan. Behavioral data were collected between December 2014 and March 2015. The total observation time was 129 h. Hair samples were collected in late March and early April 2015, and cortisol was extracted from the hair and measured with enzyme immunoassay. The hair growth rate was estimated to be 1.33 ± 0.06 cm/month. The results revealed that there was a positive correlation between the rate of receiving aggression and HC levels. We also found a significant negative correlation between the balance between giving and receiving grooming (grooming balance index: GBI), which was calculated by subtracting the rate with which grooming is given from that with which it is received, and the rate of receiving aggression and between the GBI and HC levels. Thus, individuals receiving higher levels of aggression also tended to give grooming for relatively long periods compared to the time they were being groomed. In contrast, the rate of initiating aggression did not have a relationship with either HC levels or any measure of social grooming. We did not find social buffering effects, as there was no correlation between mutual social grooming and HC levels. These results show that not only aggressive interactions but also overall social situations in which animals do not have balanced relationships with others might result in the long-term elevation of cortisol levels in captive male chimpanzees.     

Innovative social behavior in chimpanzees (Pan troglodytes)

We present evidence of agonistic buffering in captive chimpanzees, recorded from 1993 until 2005, mainly from ad libitum sampling in over 2000 hr of observation. A total of 33 agonistic buffering episodes were analyzed for context and effects of this complex social behavior. Agonistic buffering was directed at the whole chimpanzee colony as they supported an individual who initially received aggression from the alpha male, independently of the victim's age, sex or social rank. Chimpanzee agonistic buffering behavior is compared with that in other nonhuman primate species, and we describe some particularities of chimpanzee agonistic buffering: the status of the buffers used-socially important offspring such as those from the alpha female-and the social rank of the adult male responsible for the buffering episode-alpha male. Possible functions for this behavior in chimpanzees are suggested as appeasement of group members in a particularly crowded captive setting, and/or as a "forced reconciliation" mechanism. Chimpanzees exhibit behavioral flexibility by adapting themselves to new social and physical situations and use novel behavior to achieve social benefits.     

Social enhancement can create adaptive,arbitrary and maladaptive cultural traditions

Many animals are known to learn socially, i.e. they are able to acquire new behaviours by using information from other individuals. Researchers distinguish between a number of different social-learning mechanisms such as imitation and social enhancement. Social enhancement is a simple form of social learning that is among the most widespread in animals. However, unlike imitation, it is debated whether social enhancement can create cultural traditions. Based on a recent study on capuchin monkeys, we developed an agent-based model to test the hypotheses that (i) social enhancement can create and maintain stable traditions and (ii) social enhancement can create cultural conformity. Our results supported both hypotheses. A key factor that led to the creation of cultural conformity and traditions was the repeated interaction of individual reinforcement and social enhancement learning. This result emphasizes that the emergence of cultural conformity does not necessarily require cognitively complex mechanisms such as ‘copying the majority’ or group norms. In addition, we observed that social enhancement can create learning dynamics similar to a ‘copy when uncertain’ learning strategy. Results from additional analyses also point to situations that should favour the evolution of learning mechanisms more sophisticated than social enhancement.     

Reduced brain cell proliferation following somatic injury is buffered by social interaction in electric fish,Apteronotus leptorhynchus

In many species, the negative effects of aversive stimuli are mitigated by social interactions, a phenomenon termed social buffering. In one form of social buffering, social interactions reduce the inhibition of brain cell proliferation during stress. Indirect predator stimuli (e.g., olfactory or visual cues) are known to decrease brain cell proliferation, but little is known about how somatic injury, as might occur from direct predator encounter, affects brain cell proliferation and whether this response is influenced by conspecific interactions. Here, we assessed the social buffering of brain cell proliferation in an electric fish, Apteronotus leptorhynchus, by examining the separate and combined effects of tail injury and social interactions. We mimicked a predator‐induced injury by amputating the caudal tail tip, exposed fish to paired interactions that varied in timing, duration and recovery period, and measured brain cell proliferation and the degree of social affiliation. Paired social interaction mitigated the negative effects of tail amputation on cell proliferation in the forebrain but not the midbrain. Social interaction either before or after tail amputation reduced the effect of tail injury and continuous interaction both before and after caused an even greater buffering effect. Social interaction buffered the proliferation response after short‐term (1 d) or long‐term recovery (7 d) from tail amputation. This is the first report of social buffering of brain cell proliferation in a non‐mammalian model. Despite the positive association between social stimuli and brain cell proliferation, we found no evidence that fish affiliate more closely following tail injury.     

Naked Mole-Rat is Sensitive to Social Hierarchy Encoded in Antiphonal Vocalization

The maintenance of social relationships is critical for group-dwelling species. Social animals often exhibit behaviors such as antiphonal vocalizations that reduce conflict and maintain affiliations. Naked mole-rats ( Heterocephalus glaber ) have a complex hierarchical society comparable to that of bees and ants. They are also known for their extensive vocal repertoire, which may have evolved in the absence of visual cues. The most frequent vocalization used by naked mole-rats is the soft chirp (SC). It has an antiphonal nature and may function in rank identification and in maintaining affiliations. Relative body weight differences, which are directly related to social rank, are positively correlated with SC emission rates. SCs are elicited from either physical touch or the SC of another conspecific, and other cues might contribute to SC utterance. In the current study, we examined whether an SC alone was able to elicit SC responses. Specifically, we presented artificial SC-like sounds and determined whether the response rate was modulated by the acoustic properties of the stimulus. An analysis of response latency revealed that animals responded to the audio stimuli, and a single audio stimulus could elicit responses from two animals. Thus, antiphony in naked mole-rats may occur among three or more animals. We also found that animals were able to discriminate the acoustic properties of the stimulus and responded more frequently to audio stimuli resembling SCs from large animals than to those resembling SCs from small animals. Therefore, naked mole-rats may be able to judge social relationships (dominant or subordinate) based solely on SCs. The constraints of subterranean habitats and increased social complexity may have led to the evolution of this communication system.     

The influence of sex and relatedness on stress response in common marmosets (Callithrix jacchus)

Research in stress physiology has demonstrated the benefits of receiving social support during stressful conditions. However, recent data have shown that the efficacy of social support in buffering physiological and behavioral responses to stressor agents depends on species, sex, and relatedness among animals. This study investigated whether different kinds of social support (presence of same sex related or nonrelated conspecifics) have the same effect on hormonal (fecal cortisol levels) and behavioral responses (agonistic: scent-marking and individual piloerection; anxiety: locomotion; tension-reducing: autogrooming, allogrooming, and body contact). We used adult male and female isosexual dyads of Callithrix jacchus, a small Neotropical primate from the Callitrichidae family, widely used in the study of stress and related diseases. Following a 28-day baseline phase, dyads faced three challenging situations (phase 1: dyads were moved together from the baseline cage to a similar new cage; phase 2: each dyad member was moved alone to a new cage; and phase 3: dyad members were reunited in the same baseline cage). Type of social support was found to influence the response to stressors differently for each sex. Related male dyads did not change their hormonal or behavioral profile over the three experimental phases, when compared to the baseline phase. For nonrelated male dyads, social support buffered hormonal but not behavioral response. For females, the social support offered by a related and nonrelated animal, does not seem to buffer the stress response, as shown by correlations between agonistic behaviors versus cortisol and locomotion during all three experimental phases and a significant increase in fecal cortisol levels during phases 2 and 3, when compared with baseline levels. The results only partially support the buffering model theory and corroborate other studies reporting that the benefits of social support during a period of crisis arise only when it is adaptive for that species.     

Buffering capacity of bacilli that grow at different pH ranges.

Cytoplasmic buffering capacities and buffering by whole cells were examined in six bacterial species: Bacillus acidocaldarius, Bacillus stearothermophilus, Escherichia coli, Bacillus subtilis, Bacillus alcalophilus, and Bacillus firmus RAB. Acid-base titrations were conducted on whole cells and cells permeabilized with Triton X-100 or n-butanol. In all of the species examined, the buffering capacity of intact cells was generally a significant proportion of the total buffering capacity, but the magnitude of the buffering capacity varied from species to species. Over the entire range of pH values from 4 to 9.5, B. subtilis exhibited a cytoplasmic buffering capacity that was much higher than that of B. stearothermophilus, B. acidocaldarius, or E. coli. The latter three species had comparable cytoplasmic buffering capacities at pH 4 to 9.5, as long as optimal conditions for cell permeabilization were employed. All of the nonalkalophiles exhibited a decrease in cytoplasmic buffering capacity as the external pH increased from pH 5 to 7. At alkaline pH values, the two thermophiles in the study had particularly low cytoplasmic buffering capacities, and the two alkalophilic bacteria had appreciably higher cytoplasmic buffering capacities than any of the other species studied. Cytoplasmic buffering capacities as high as 1,100 nmol of H+ per pH unit per mg of protein were observed in alkalophilic B. firmus RAB. Since previous studies have shown that immediate cytoplasmic alkalinization occurs upon loss of the active mechanisms for pH homeostasis in the alkalophiles, the very high buffering capacities apparently offer no global protection of internal pH. Perhaps, the high buffering capacities reflect protective mechanisms for specific macromolecules or process rather than part of the mechanisms for bulk pH homeostasis.