FRANKLIN D. MCMILLAN

Best Friends Animal Society, Kanab, Utah, USA

A large literature now exists to affirm that social animals ¹ – human and nonhuman – have a fundamental biological need to form emotional connections with others and that they experience distress when socially isolated or separated from other valued individuals (Panksepp, 1998; Hostinar and Gunnar, 2015; McMillan, 2016). The evolutionary value of sociality – for parental care, food and other resource acquisition, mate selection, and predator defenses – has been extensively reviewed (Alexander, 1974). This chapter addresses the positive effects of social affiliation that extend beyond these fitness benefits.

Current evidence convincingly demonstrates that social mammals (including humans, as well as some nonmammalian species) share a distinct attribute, referred to as social support, whereby individuals in the company of affiliative conspecifics experience improved physical and psychological well-being (Kikusui et al., 2006; Rault, 2012). There is currently no universally agreed upon definition of social support (Uchino, 2006). Some definitions limit the benefits to times of stress; for example, social support has been defined as ‘a social network’s provision of psychological and material resources intended to benefit an individual’s ability to cope with stress’ (Hostinar and Gunnar, 2015). However, as we will see, the benefits of social contact and social support occur prominently – but not exclusively – during times of stress (Taylor et al., 2005) and, accordingly, social support in this chapter will use the definition inclusive of all benefits derived from social interactions both within and outside of stressful contexts. The subset of social support that functions during and shortly after stressful conditions is termed social buffering (or stress buffering), and refers to the phenomenon in which individuals experience less overall stress and/or recover more rapidly from stress when in the presence of compatible conspecifics than when not (Kikusui et al., 2006; Hennessy et al., 2009).

8.1.2 Health benefits

Physical health

One of the most robust empirical findings regarding social support in humans and nonhuman animals (hereafter ‘animals’) is its association with physical health and mortality (Hawkley et al., 2012). In humans, hundreds of empirical investigations have demonstrated ties between social support and reduced health risks of all kinds and involving all major body systems (e.g., cardiovascular, endocrine, and immune), affecting both the initial likelihood of disease as well as the course of recovery among those who are already ill (Uchino et al., 1996; Taylor et al., 2005). In animal species, a small sampling of adverse effects of social isolation on physical health include exacerbation of coronary artery atherosclerosis among female long-tailed macaques, promotion of the development of obesity and type 2 diabetes in mice, exacerbation of infarct size and edema and decreased post-stroke survival rate following experimentally induced stroke in mice, neuroinflammation and cell death following experimental cerebral ischemia, and detrimental neurological changes (reviewed by Cacioppo et al., 2011, 2014a). In addition, when compared with people who report having meaningful social bonds with others, people who perceive themselves as socially isolated or lacking strong connections with others have a significantly shorter lifespan (Cacioppo and Patrick, 2008; Cacioppo and Hawkley, 2009), and social animals who form strong relationships and are integrated most strongly into group living are most likely to survive, reproduce, and raise offspring to reproductive age (MacDonald and Leary, 2005).

Mental health

In addition to the benefits to physical health, empirical investigations spanning the past century support the notion that social ties and social support in humans are positively correlated with improved mental health and psychological well-being (Achat et al., 1998; Ethgen et al., 2004; Thoits, 2011; Rault, 2012; Hostinar and Gunnar, 2015). Social connections predict decreased negative affect (Siedlecki et al., 2014) and can lessen the risk of anxiety and depression (Kikusui et al., 2006; Neumann, 2009; Thoits, 2011; Siedlecki et al., 2014) as well as promote the positive aspects of mental health (Feeney and Collins, 2015). In studies looking at the relationship between social relationships and the more general well-being concepts, social support was determined to be associated with improved quality of life (Bennett et al., 2001), subjective well-being (Feeney and Collins, 2015), and life satisfaction (Siedlecki et al., 2014).

Stress is the most readily recognized factor connecting social inclusiveness and enhanced mental health and well-being. Evidence in humans indicates that social support buffers the harmful mental health impacts of stress exposure (Thoits, 2011; Smith and Wang, 2014) and that during stressful events receiving caring support from social partners increases feelings of calmness and security, decreases depression and anger, and increases positive mood (Feeney and Collins, 2015).

Research has elucidated the stress buffering effect of social support. Stress responses comprise an adaptive mechanism that enables biological organisms to respond to changes in the environment, with the hypothalamic–pituitary–adrenocortical (HPA) axis being widely regarded as the body’s primary stress-responsive neuroendocrine system (Hennessy et al., 2009; Rault, 2012). A broad array of aversive and/or arousing situations elicit increased HPA activity, which in the short-term promotes successful coping (greater resilience) with stressors (Hennessy et al., 2009). However, repeated or prolonged HPA activation is associated with mental disturbances, emotional dysfunction, and psychopathological conditions such as depression (Taylor et al., 2005; Ditzen and Heinrichs, 2014).

Knowledge of the connection of social factors and stress dates back to the 1950s. In a literature review, Bovard (1959, p.269) concluded that, ‘Taken together, these studies at the human and animal levels suggest presence of another animal of the same species has protective effect under stress’. Seeman and McEwen (1996) reviewed the animal and human studies between the 1960s and mid-1990s for evidence of social environment influencing neuroendocrine reactivity, including effects on activity of the HPA axis, sympathetic nervous system (SNS), and cardiovascular system. The key finding of the reviewed studies was that positive social relationships can attenuate patterns of neuroendocrine responses to stressors: both HPA and SNS activity are dampened during and briefly following stressful experiences (reviewed by Seeman and McEwen, 1996). Subsequent research has produced ample evidence to confirm these findings in humans and animals (reviewed by Kikusui et al., 2006; Hennessy et al., 2009; Rault 2012; Hostinar et al., 2014; Hostinar and Gunnar 2015; Sullivan and Perry 2015).

Evidence demonstrating that social support dampens physiologic stress responses converges well with a line of research examining how animals behave when exposed to stress. A large body of work now exists to show that in general, a stressed social animal (human and nonhuman) is highly attracted to conspecifics and that seeking social proximity or social contact and acquiring such contact can lead to a reduction in their stress hormone levels and distress vocalizations (Rault, 2012; Hostinar et al., 2014; Smith and Wang, 2014). As just one example, Coe et al. (1982) found that when monkeys were exposed in pairs to the fear-inducing stimulus of a snake they exhibited a strong preference for staying in close proximity with each other. These findings have led to the suggestion that social buffering may be a crucial component of the motivation underlying formation and maintenance of social relationships, since stress alleviation would be expected to be reinforcing (Hennessy et al., 2009; Hostinar et al., 2014).

8.2 Social Support and Social Buffering in Animals

8.2.1 How social support benefits mental health and well-being

Categorizing the effects of social support

The analysis of social support benefits is hampered by the existence of multiple methods of subdividing and categorizing the important constructs. In addition, all methods of categorization yield overlaps and indistinct lines between the different divisions (see Fig. 8.1). The two major methods of subdividing the positive social support effects are stress-related versus nonstress-related and isolation-related stress versus nonisolation-related stress.

STRESS-RELATED VERSUS NONSTRESS-RELATED EFFECTSThe social support literature has focused on stress buffering effects of social support (resulting in the aforementioned occurrence of some definitions of social support confining the effects to a stress context). However, numerous studies have indicated that social support can protect and promote well-being both when individuals are and are not experiencing stress (Thoits, 2011; Feeney and Collins, 2015). That social support is beneficial in the absence of adversity led to new thinking, one influential approach being that of Cohen and Wills (1985), who proposed that social support refers to two theoretical mechanisms. The main effects hypothesis states that social support exerts positive effects on well-being irrespective of stressors (Fig. 8.1). In this way, there is a direct relationship between well-being and social support: the more social support an individual has, the better the well-being, regardless of the individual’s level of stress. Here, the relation between quality of life and social support is linear (Helgeson, 2003; Ditzen and Heinrichs, 2014). In contrast, the social buffering hypothesis views social support as operational and beneficial only during episodes of stress and adversity, reducing the impact of stressors on the individual’s well-being (Fig. 8.1). Under these effects the individual’s level of stress or adversity determines the relation of social support to well-being: in the absence of stress, well-being is independent of social support, whereas in instances of adversity, well-being is enhanced by the stress-buffering effects of social support (Helgeson, 2003; Rault, 2012). There is evidence to support the existence, as well as the coexistence, of both mechanisms (Cohen and Wills, 1985; Ditzen and Heinrichs, 2014).

The existence of the social buffering effects is well documented empirically in both animals (Rault, 2012) and humans (Kikusui et al., 2006); however, in animals the main effects hypothesis has received virtually no attention by researchers until quite recently. Wittig et al. (2016) tested the main effects and social buffering hypotheses by measuring urinary glucocorticoid levels in wild chimpanzees with or without their bond partners in three situations: a natural stressor, everyday affiliation, and resting. Results showed HPA axis dampening during daily engagement with bond partners both within and outside of stressful contexts, thereby supporting the existence of a main effects mechanism. This is consistent with substantial research demonstrating that when social animals are permitted to interact with conspecifics they had decreased plasma glucocorticoid levels (reviewed by Kikusui et al., 2006; DeVries et al., 2007). These findings suggest that the well-being of nonhuman animals may benefit from social support during all aspects of life, not simply during times of stress.

ISOLATION-RELATED AND NONISOLATION-RELATED STRESSIf we consider the stress-related benefits of social support, there are two types of stress that are relevant: that associated with and that not associated with social isolation. Because social isolation is itself a stressor (see next section) some confusion exists when social buffering operates in situations of isolation. The presence of social companions generally has, by its very nature, an alleviating effect on such isolation stress. The question, then, is whether social interaction in this context constitutes a ‘true’ buffering effect on neuroendocrine stress systems, or simply eliminates the stressor itself by reestablishing social interaction. As generally conceived, social buffering refers to the capacity of an animal to cope with a broader array of stressful challenges – isolation-related as well as nonisolation-related – when accompanied by conspecifics (Rault, 2012). As Rault (2012) has noted, the presence of partners has more to contribute to an animal’s well-being than simply nullifying social separation distress.

With the addition of a third factor – the elaboration of pleasant feelings (discussed in the ‘Promotion of positive affect’ section, p. 104) – we can now configure the above subdivisions of social support into three major components that comprise the connection between social factors and well-being: (i) alleviation of negative affect (including stress) of social separation or isolation; (ii) buffering of nonsocial-isolation stress and adversity; and (iii) promotion of positive affect (see Fig. 8.1).

Alleviation of negative affect (including stress) of social separation or isolation

Given the crucial importance of social connectedness in group-living species, there is a clear adaptive benefit to having a strong aversive response upon social separation as a potent motivator of social connection or reconnection (Eisenberger, 2012; Cacioppo et al., 2014a), just as there is a benefit to having negative affect signaling and motivating corrective behavior for other conditions threatening survival, such as thirst, hunger, and tissue damage (MacDonald and Leary, 2005; Cacioppo et al., 2006, DeWall et al., 2010). Panksepp (2011) contends that research in humans and animals now strongly supports the notion that emotional pain arising from the disruption of social relationships – whether it be through the loss of contact with or death of a social partner – is a basic emotional response of mammalian brains. Social separation and/or isolation has been shown to rank among the most reliable and potent stimuli for producing a stress response in a diverse array of social mammals (reviewed by Cacioppo et al., 2011, 2014b, 2015a; Hawkley et al., 2012; Rault 2012), and is widely used as an experimental model for inducing stress (Cacioppo et al., 2014b) (Fig. 8.2).

The adverse affective experience associated with social separation (referred to as social pain) is actually composed of a number of different emotions (reviewed by McMillan, 2016), each demonstrated to have powerful adverse effects on mental health and well-being across phylogeny. In humans and animals, loneliness and social isolation distress result when, respectively, an individual’s actual level of social relationships – in terms of quality and/or quantity – fails to match their desired level of relations and from objectively being alone (Weiss, 1973; Cacioppo et al., 2014b, 2015a,b; Capitanio et al., 2014). In this way, an individual person or animal could experience loneliness when separated from desired partners, even if in the company of other conspecifics (Capitanio et al., 2014). Accumulating research suggests that fear is a component of the negative affect of social pain (reviewed by McMillan, 2016). Being socially separated presents a survival risk (e.g., from predation, health disorders), and current evidence indicates that the brain of social animals evolved mechanisms to put individuals into a short-term, self-preservation mode when they find themselves without companionship or mutual protection/assistance (Cacioppo et al., 2015b). Indeed, the brain’s social and fear circuitry share the amygdala as a core structure, so social relationships and fear modulation appear to be closely related (Panksepp, 2001). Overlapping the research noted earlier that in stressful situations animals seek the company of others, fear increases rats’ preference for conspecific contact and appears to be allayed when conspecific animals are together, suggesting that fear reduction may contribute to the forces of social attraction between individuals (Kikusui et al., 2006).

Specific adverse mental health effects include social separation in adulthood producing behavioral indicators of depression or anxiety in a number of species (Grippo et al., 2007). Currently, chronic social isolation serves as an animal model for studying elicitation, course trajectory, and treatment responses of affective disorders in several species (reviewed by Capitanio et al., 2014; Cacioppo et al., 2015b). For example, in prairie voles the absence of social contact can cause dysregulation of HPA axis activity and produce behaviors that mimic symptomatology of depression and anxiety disorders in humans (Smith and Wang, 2014). Taken together, current evidence indicates that social separation and isolation are risk factors for impaired mental health and the development of psychopathologies (Neumann, 2009) (see Fig. 8.3).

Social pain is elicited whenever the level of social interaction is inadequate to meet an individual’s needs, which can include separation from a specific social partner, from any social partner, or complete isolation. The ways social pain is alleviated vary correspondingly, in accord with the nature of the social deprivation eliciting emotional distress. In addition, specific modulating factors (presented in ‘Factors modulating the efficacy of social buffering’ section) influence how social companionship alleviates social pain and benefits mental health and well-being. Interestingly, some research suggests that alleviating the distress of social pain requires only a reasonable facsimile of the missing social element. For example, da Costa et al. (2004) demonstrated that simply providing a picture of a conspecific’s face to an isolated adult sheep caused major reduction in the animals’ behavior, autonomic, and endocrine stress responses.

Buffering of nonsocial-isolation stress and adversity

Evidence accumulating over the past 50 years demonstrates the buffering effect of social support for stress and adversity unrelated to social deprivation. Positive effects have been documented in two major groups of animals: the young (infants and juveniles) and adults. Stress buffering in these two groups may or may not involve the same neurobiological mechanisms.

INFANT AND JUVENILE ANIMALSThe most extensively investigated form of social buffering is that exerted by the mammalian mother on her infant’s stress responses (Hennessy et al., 2009). Rat pups (Hostinar et al., 2014) and goat kids (Liddell, 1949) exposed to a stressor exhibit less physiological and behavioral signs of stress when the mother is present compared to when she is not. Stress buffering in the young has been demonstrated in nonhuman primates in several studies (reviewed by Kikusui et al., 2006). For example, when squirrel monkey infants were separated from their mother they showed a lower HPA axis response if they remained in the company of their social group, indicating that the conspecific companions acted as a buffer to maternal separation stress. Similarly, when infants are exposed to the stress of separation from their social companions, the presence of the mother blunts the elevation of cortisol levels that occur in the mother’s absence.

While social buffering of the HPA axis in early life has been studied most extensively in mammals (Hennessy et al., 2009), recent work has begun to include avian species. Edgar et al. (2015) compared stress responses of chicks in the presence and absence of their mother and found that mother hens are able to buffer their chicks’ stress response to an aversive stimulus such as a puff of air.

ADULT ANIMALSResearch methodology for studying social buffering in adult animals have varied widely in terms of species (e.g., numerous mammalian orders), type of stressor (e.g., electric shock, white noise, exposure to a novel environment, social defeat by a dominant conspecific, exposure to a live snake, and human encounter), and timing of the support relative to stressor exposure (e.g., before, during, or after) (Rault, 2012). The following represents a relatively small sampling of the research in this field.

Livestock animals – Sheep exposed to a stressful fear eliciting stimulus (sudden opening of umbrella) showed fewer behavioral signs of reactivity (attempts to escape and fast movements) if in a group than if socially isolated (González et al., 2013). Lower stress levels (measured by behavior and cortisol levels) occurred in bulls during pre-slaughter handling if maintained in physical or visual contact with their familiar social group (Mounier et al., 2006). Fear-inducing stimuli elicit fewer behavioral signs of disturbance in heifers when near companion peers (Boissy and Le Neindre, 1990). In horses, the stress of stabling for the first time – as indicated by behaviors such as neighing, pawing, nibbling, snorting, and stereotypies – was significantly less in horses with companions than those without (Ditzen and Heinrichs, 2014). When horses were transported by trailer, those traveling with a companion showed significantly reduced physiological responses than those traveling alone (Kay and Hall, 2009).

Rodents – In prairie voles, immobilization-induced increases in stress-related behaviors and corticosterone levels occurred in females recovering from the stressor alone, but not if recovering with their male partner (Smith and Wang, 2014). Davitz and Mason (1955) reported that rats showed a lesser degree of immobilization when shocked in the presence of a companion than when shocked alone. Training rats with electric shock as punishment was less effective when the subject rat was accompanied by conspecifics than when trained alone (Rasmussen, 1939). Rats exposed to a fear stimulus or a novel environment showed fewer indicators of fear, such as fearful withdrawal behavior and a lower corticosterone response, if with a partner rat than when alone (Davitz and Mason, 1955; Taylor, 1981; Kikusui et al., 2006) (Fig. 8.4). Similarly, following forced exposure to a novel environment, group-housed mice showed a significantly lower increase in corticosterone levels than did solitary-housed mice (Bartolomucci et al., 2003). Isolated rats, as compared to socially housed rats, show significantly greater corticosterone responses to restraint stress (Hermes et al., 2006). Immobilization and cold stress elicits greater reactivity of the HPA axis in isolated rats than in rats housed in groups (Dronjak et al., 2004). Rats tested alone in a chronic approach-avoidance conflict situation showed significantly greater gastric ulceration than rats tested with companions present (Conger et al., 1958). Ruis et al. (1999) found that if rats are isolated after social defeat by a dominant rat they will show long-lasting, anxiety-like behavioral and physiological changes, but if placed with familiar rats these adverse effects are greatly reduced.

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