Urinary oxytocin levels in relation to post-conflict affiliations in wild male chimpanzees (Pan troglodytes verus)
Introduction
Living in social groups provides benefits such as increased access to mating partners and feeding resources as well as a lower risk of predation and infanticide (Krause and Ruxton, 2002; Sterck et al., 1997; Van Schaik, 1983; Wrangham, 1980). Yet, living in a social group confronts an individual with numerous challenges as well, including increased risk of disease transmission and competition over food, mates or social partners (Krause and Ruxton, 2002; Sussman and Chapman, 2004; Van Schaik, 1983). Competition between group members can therefore escalate into aggressive conflicts, which induces social tension and may disturb group cohesion and cooperative tasks when former opponents increase spatial distance or even leave the group (Aureli, 1997; Aureli et al., 2002; Cheney and Seyfarth, 1997; Cords, 1992; Das et al., 1998; De Waal, 2000a; Wittig and Boesch, 2005). Thus, the dilemma of social living is that individuals compete with the same individuals they need to cooperate with to gain the benefits of being in a group (De Waal, 2000a). While behavioral mechanisms contributing to living in a stable group have been investigated in numerous animal species, few studies have examined proximate mechanisms facilitating behaviors needed to maintain a stable social group.
Aggressive conflicts are costly and socially disruptive events for both aggressor and victim, since they result in relationship uncertainty between former opponents and loss of predictability of future interactions (Aureli, 1997; Aureli et al., 1999; Cords, 1992; Das et al., 1998; De Waal, 2000b, De Waal, 1989, De Waal, 1986; Fraser et al., 2009; Palagi and Norscia, 2011; Sapolsky, 2005, Sapolsky, 1992; Wittig et al., 2015; Wittig and Boesch, 2005). To overcome the disruptive effects of conflicts many social animals have developed friendly post-conflict (PC) interactions with group members, such as reconciliation (Aureli and De Waal, 2000). Reconciliation is an affiliative interaction between former opponents which occurs after an aggressive conflict (De Waal and van Roosmalen, 1979). Behavioral studies have shown that reconciliation has a calming or anxiety reducing effect (Aureli, 1997; Butovskaya et al., 2005; Das et al., 1998; Palagi and Norscia, 2011). Reconciliation functions to reduce uncertainty about future interactions between opponents (‘uncertainty-reduction’ hypothesis) by reducing the risk of further aggression and therefore repairs the opponents' relationship (‘relationship repair’ hypothesis) by restoring tolerance levels between former opponents (Aureli, 1997; Butovskaya et al., 2005; Cords, 1992; Das et al., 1998; Koyama, 2001; Palagi and Norscia, 2011; Wittig and Boesch, 2005). Reconciliation is observed more frequently between individuals that share a valuable relationship (‘valuable relationship’ hypothesis) suggesting that reconciliation is a social strategy used by individuals when they have the most to gain from repairing a relationship (Aureli, 1997; Aureli et al., 2002; Cords, 1992; Koski et al., 2007; Wittig and Boesch, 2005, Wittig and Boesch, 2003).
Reconciliation, however, is not the only form of affiliation that can occur after a conflict. Another important PC affiliation is an affiliation offered by a previously uninvolved third party or ‘bystander’ to one of the former opponents (Call et al., 2002; De Waal and van Roosmalen, 1979; Palagi et al., 2004; Fraser et al., 2009). Consolation is a PC affiliation directed from an uninvolved bystander to the former recipient of an aggression (De Waal and van Roosmalen, 1979), while a PC affiliation directed from an uninvolved bystander to the former aggressor is termed appeasement (De Waal and Aureli, 1996; Romero et al., 2011). In chimpanzees, suggested but mutually non-exclusive functions of consolation include social support (true consolation), third party relationship repair, and self-protection (Fraser et al., 2008, Fraser et al., 2009; Fraser and Bugnyar, 2010; Koski and Sterck, 2009; Romero et al., 2010; Wittig and Boesch, 2010). To distinguish among these different functions it is important to consider the relationship quality between the bystander and the former opponents (Fraser et al., 2009). Consolation that functions: (1) to support a distressed valuable partner is offered by a valuable partner, (2) to repair the relationship of former opponents is offered by a valuable partner of the former opponent, and (3) to self-protect a bystander is offered to former opponents by individuals which are frequent targets of redirected aggression (Fraser et al., 2009; Koski and Sterck, 2009). The underlying motivation of the bystander offering consolation to a valuable partner is suggested to be sympathetic concern (De Waal, 2012; Fraser et al., 2008; Palagi et al., 2014). Bystander initiated PC affiliations directed towards aggressors (appeasement) have been suggested to differ in motivation and function from PC affiliations directed to victims of a fight (Das et al., 1998; Fraser et al., 2009; Romero et al., 2011). A study in captive chimpanzees specifically investigating bystander PC affiliations directed to aggressors, concluded that this PC affiliation might serve as a mechanism to reduce the spread of aggression throughout the group, or similarly to consolation might have the function to support a valuable partner (former aggressors) which could be a mechanism to strengthen a bond (Romero et al., 2011).
The adaptive consequences of PC affiliations, like the reduction of future aggression, anxiety and uncertainty, as well as the reestablishment of cooperative and social relationships, have been investigated in numerous animal species, while little effort has been made to understand endocrinological mechanisms underlying affiliative conflict resolution behavior. Social uncertainty, as well as repeated exposure to psychosocial stressors like aggression or loss of status, has been shown to lead to short-term or enduring activation of the Hypothalamic-Pituitary-Adrenal (HPA) axis, especially when coping mechanisms are not available (Bartolomucci et al., 2005; Korte et al., 2005; Wittig et al., 2015). A common measure of HPA axis activity is the investigation of changes in glucocorticoid levels. The uncertainty reduction function of reconciliation has been examined in human children through the comparison of glucocorticoid levels after reconciled and non-reconciled conflicts (Butovskaya et al., 2005). Children had significantly higher salivary glucocorticoid levels after unreconciled than after reconciled conflicts, and reconciliation resulted in the reduction of anxiety induced by the former conflict (Butovskaya et al., 2005). While reconciliatory uncertainty reduction has been measured both on a behavioral and physiological level, the relationship repair function of reconciliation and the social support or bond strengthening function of bystander PC affiliation has mainly been studied on a behavioral level (Aureli, 1997; Butovskaya et al., 2005; Call et al., 2002; Cords, 1992; Das et al., 1998; Fraser et al., 2008; Wittig and Boesch, 2005, Wittig and Boesch, 2010). Consequently, much less is known about underlying endocrinological mechanisms of PC affiliations as means of relationship repair and social support.
Endocrine systems rarely act in isolation (Gangestad and Grebe, 2017). It is therefore likely that in addition to the HPA axis other hormonal systems are activated after aggressive conflicts or during PC affiliations, potentially involved in relationship repair, social support and bond strengthening functions of PC affiliations. A possible candidate is the oxytocinergic system, which has been shown to be involved in a variety of social behaviors and processes including affiliative and approach behaviors, bond maintenance and social support, all of which are central elements of PC affiliations (Carter, 1998; Insel and Young, 2001; Crockford et al., 2013; Williams et al., 1994; Gordon et al., 2011; Ross et al., 2009; Snowdon et al., 2010; Lukas et al., 2011; Smith and Wang, 2014). Central and/or peripheral release of oxytocin has been found in response to physical and psychosocial stressors as well as fearful contexts in rodents, non-human primates and humans (Hinde et al., 2016; Neumann and Slattery, 2016). Hence, physical and psychosocial stressors have been shown to activate both the HPA axis and the oxytocinergic system (Brown et al., 2016; de Jong et al., 2015; Hinde et al., 2016; Lang et al., 1983; Torner et al., 2017). In addition, numerous studies demonstrate that the oxytocinergic system interacts with the HPA axis (Neumann and Landgraf, 2012). Naturally and experimentally elevated oxytocin levels after or during stressor exposure in combination with social support have been found to attenuate the perception of a stressor and to reduce anxiety (Grewen et al., 2005; Heinrichs et al., 2003; Seltzer et al., 2010; Ziegler and Crockford, 2017). Receiving social support during or after exposure to a stressor has been shown to facilitate the recovery from an aversive experience, a phenomenon termed ‘social buffering’ (Cohen and Wills, 1985; Kikusui et al., 2006). The oxytocinergic system has been identified as a key facilitator of social buffering effects (French et al., 2017; Smith and Wang, 2014).
The oxytocinergic system's effects on approach and affiliative behavior during stressful situations are suggested to be mediated through its anxiolytic effects (Carter, 1998; Feldman, 2012; Neumann, 2008). Elevated oxytocin levels have been associated with reduced perception of threatening social stimuli which may induce feelings of safety and thus facilitate approach and affiliative interactions (Feldman, 2012; Kirsch, 2005; Kosfeld et al., 2005; Lukas et al., 2011; Radke et al., 2017). Additionally, the oxytocinergic system is suggested to affect motivational states related to affiliation and social bonding through its connectivity with the dopaminergic reward system (Bartz et al., 2011; Gordon et al., 2011). Thus, increased activity of the oxytocinergic system after or during stressor exposure might enhance the motivation to affiliate with a social partner in order to receive social support (Cavanaugh et al., 2016; Taylor, 2006). Accordingly, the oxytocinergic system's role in reconciliations and bystander PC affiliations could be to enhance the motivation to affiliate and/or to facilitate affiliative behavior through its anxiolytic effects. In both cases elevated oxytocin levels might be expected after aggressive conflicts that are followed by PC affiliations. However, if the oxytocinergic system is activated in response to potential social or energetic stressors, such as aggressive conflicts, elevated oxytocin levels might be associated with aggressions independent of PC affiliations.
The oxytocinergic system might also be involved in the modification of behavioral responses following a conflict. The ‘social salience’ hypothesis states that oxytocin increases the sensitivity to social cues, resulting in enhanced sensitivity to emotional stimuli, independent of their valence (Bartz et al., 2011; Domes et al., 2007; McQuaid et al., 2014; Shamay-Tsoory et al., 2009). By identifying overarching patterns across studies, it was proposed that the oxytocinergic system promotes anxiety and aggressive behaviors in response to unpredictable threats and competitive situations, but stimulates affiliative behaviors in response to positive supportive and familiar contexts (De Dreu and Kret, 2016; Shamay-Tsoory and Abu-Akel, 2016). Thus, whether prosocial or anti-social effects are facilitated by the oxytocinergic system strongly depends on the social situation and inter-individual differences (Bartz et al., 2011; Crockford et al., 2014; Olff et al., 2013). In line with the ‘social salience’ hypothesis, the oxytocinergic system might, therefore, be activated after aggressive conflicts, even after those that are not followed by affiliation.
Finally, the oxytocinergic system could also be involved in the relationship repair function of reconciliation through mechanisms associated with bond maintenance, since the oxytocinergic system plays a crucial role in the formation and maintenance of social bonds (Carter, 1998; Feldman, 2012; French et al., 2017; Insel and Young, 2001; Ross and Young, 2009). Social bonds are formed and maintained through repeated affiliative contacts and positive social behaviors (Carter, 1998; Uvnäs-Moberg, 1998). The quality of social relationships is positively associated with oxytocin levels and rates of affiliative and sexual behaviors in monogamous primates and grooming in chimpanzees (Crockford et al., 2013; Finkenwirth et al., 2015; Snowdon et al., 2010). Similar patterns have been found in humans (Feldman et al., 2010; Grewen et al., 2005; Holt-Lunstad et al., 2015; Light et al., 2005). Additionally, elevated activity of the oxytocinergic system has been found following mate separation in monogamous prairie voles and titi monkeys (Bosch et al., 2016; Hinde et al., 2016), as well as after pair-mate reunion (Hinde et al., 2016). Separation from a social partner may function to stimulate partner-seeking behavior which could be an additional mechanism of bond maintenance facilitated by the oxytocinergic system (Bosch et al., 2016; French et al., 2017). Likewise, humans experiencing uncertain or disturbed relationships have elevated oxytocin levels (Grebe et al., 2017). The latter authors proposed an ‘identify and invest’ hypothesis under which the oxytocinergic system is activated in relation to challenges or actual threats to a valued relationship to facilitate coping mechanisms to rescue or maintain the threatened relationship (Gangestad and Grebe, 2017; Grebe et al., 2017). Relationship repair through reconciliation could be an example of such a coping mechanism facilitated by the oxytocinergic system. Thus, in accordance with the oxytocinergic systems involvement in bond maintenance, elevated oxytocin levels might be associated with both aggressive conflicts that disturb social relationships and reconciliations between valuable partners.
In this study we combined detailed behavioral observations of wild male chimpanzees (Pan troglodytes verus) with direct, non-invasive urinary oxytocin (uOT) measurements. Since PC affiliations occur more often in males having up to 14 times higher aggression rates than females (Muller, 2002; Wittig and Boesch, 2003), we decided to only select males as focal individuals to maximize urine sample collection after single behavioral events. In a first step, we examined conciliatory and affiliative tendencies of focal individuals involved in aggressive conflicts to demonstrate the occurrence of reconciliation and bystander PC affiliation in our study groups. We therefore quantified the frequency of aggressions followed by reconciliations or bystander PC affiliations that were initiated sooner than dyadic (reconciliation) and non-dyadic (bystander PC affiliation) affiliation baselines, respectively (Veenema et al., 1994; Wittig and Boesch, 2003, Wittig and Boesch, 2005). Second, we tested the ‘valuable relationship’ hypothesis of reconciliation and investigated if aggressive conflicts are reconciled more often when opponents share a valuable relationship. Third, due to the oxytocinergic systems involvement in social buffering and bond maintenance and its anxiolytic, motivational and social salience enhancing effects we hypothesized that the oxytocinergic system is part of the relationship repair function of reconciliation and the social support/bond strengthening function of bystander PC affiliation.
We therefore compared uOT levels of individual chimpanzees after naturally observed aggressions not followed by affiliations (aggressions alone), aggressions followed by affiliation between former opponents (reconciliation), and aggressions followed by an affiliation initiated by an uninvolved bystander to one of the former opponents (bystander PC affiliation) with two control conditions: affiliations without previous aggression (affiliations alone) and after time periods without social interactions (non-social control). We formulated our predictions in accordance with the oxytocinergic systems' involvement in different behavioral processes outlined above, and distinguished between possible associations of the oxytocinergic system with aggressive and/or affiliative behavior. Due to the oxytocinergic system's potential activation in response to physiological and psychosocial stressors and social salience enhancing effects we predicted higher uOT levels after aggressions alone than after the non-social control condition. In accordance with the oxytocinergic system's involvement in social buffering, affiliative and approach behavior, as well as bond-maintenance we predicted higher uOT levels after aggressive conflicts followed by reconciliations and bystander PC affiliations than after the non-social control condition and affiliations alone. Furthermore, based on previous findings in chimpanzees and in relation to the oxytocinergic system's involvement in bond maintenance, we predicted a positive association between uOT levels and the relationship quality of PC affiliation partners. In addition, previous findings in chimpanzees revealed that reconciliations of short and long duration had the same, positive effect on the reestablishment of tolerance between former opponents (Wittig and Boesch, 2005) and variation in grooming duration of grooming bouts with a minimum length of 10 min had no effect on uOT levels (Crockford et al., 2013; Samuni et al., 2017). Thus, we predicted that changes in uOT levels in relation to PC affiliations should be independent of the duration of the affiliative interaction, if they indeed function in relationship repair, signaling social support or bond strengthening.
Section snippets
Data collection
Data were collected from two habituated chimpanzee groups at the Taï National Park, Côte d'Ivoire (5°52′N, 7°20′E), between September 2014 and May 2015 (Wittig, 2018). AP & LS conducted all-day focal animal sampling (Altmann, 1974) on all males >11 years old (N = 10 males, age 12–37; 5 males in each group) for a total of 1361 observation hours in East group and 1284 h in South group. During focal follows, we collected urine samples and recorded all social interactions and changes in activity
Demonstrating the occurrence of reconciliation and bystander PC affiliation
Out of 443 conflicts, 69 were followed by reconciliation. Thus, 16% of conflicts were reconciled. Reconciliations were initiated with a median latency of 1.2 min after aggressions (range = 0.02–224.45 min) and 78% of reconciliations (N = 54) were initiated within 10 min. The average CCT of reconciliations of all focal individuals (N = 10) was 11.73% ± 6.63 (mean ± SD; see Appendix for individual CCT values, Table A6). Out of 443 conflicts, 78 were followed by bystander PC affiliation (18%;
Discussion
Two key goals of this study were to determine whether the oxytocinergic system is involved in relationship repair processes of reconciliations and is activated in receivers of bystander initiated PC affiliations. In accordance with our predictions, based on the oxytocinergic system's involvement in social buffering, affiliative and approach behavior, as well as bond-maintenance, we found that uOT levels were higher following reconciliations and receiving bystander PC affiliations than uOT
Conclusions
In line with previous studies, we found support for the ‘valuable relationship’ hypothesis, which indicates that repairing a valuable relationship is a relevant function of reconciliation applied by the male chimpanzees in our study. Affiliative social interactions were associated with higher peripheral oxytocin levels, whether occurring as reconciliation, bystander PC affiliation or affiliation alone, than uOT levels after aggression alone and non-social control periods. Affiliative
Acknowledgements
We thank the Ivorian Ministry of Environment and Forests and Ministry of Higher Education and Scientific Research, the Office Ivoirien des Parcs et Reserves of Côte d'Ivoire and the Centre Suisse de Recherches Scientifiques. We thank Anne-Sophie Crunchant for fieldwork support, Sylvain Lemoine and all staff members of the Taï Chimpanzee Project for assistance in the field, Christophe Boesch for his continued support and advice, Roger Mundry for statistical counsel and helpful comments and Ammie
Funding
AP, AM, LS, CC, RMW were supported by the Max Planck Society; AP was supported by the Leakey Foundation; LS was supported by the Minerva Foundation; AM was supported by the Wenner Gren Foundation (9095). CC and RMW were supported by the European Research Council (ERC) (Grant Agreement No 679787). The study has benefited from discussions within the DFG Researcher Unit (FOR 2136) ‘Sociality and Health in Primates’ (grant to RMW: WI 2637/3-1). The Max Planck Society has funded research at the Taï
Ethics statement
Permissions to conduct the research was granted by the Ministries of Research and Environment of Ivory Coast and Office Ivorien des Parcs et Reserves. Methods were approved by the Ethikrat der Max-Planck-Gesellschaft.
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