Tuesday, May 18, 2010

Do Ravens Show Consolation? Responses to Distressed Others

http://img.dailymail.co.uk/i/pix/2008/05_02/ravenL0405_468x312.jpg

We already know that crows and ravens (and most corvids) are among the smartest non-human creatures in nature (smarter than most of the higher primates - and all members of the AZ legislature), but now we know that they also are compassionate and show empathy toward each other following a threat or crisis. This is considered a higher order emotional behavior reserved for the more social creatures.


Citation:
Fraser ON, Bugnyar T. (2010). Do Ravens Show Consolation? Responses to Distressed Others. PLoS ONE 5(5): e10605. doi:10.1371/journal.pone.0010605

Here is the abstract and a little bit of the article, which is open access and free online.

Do Ravens Show Consolation? Responses to Distressed Others

Orlaith N. Fraser1*, Thomas Bugnyar1,2

1 Department of Cognitive Biology, University of Vienna, Vienna, Austria, 2 Konrad Lorenz Forschungstelle, GrĂ¼nau, Austria

Abstract

Background

Bystander affiliation (post-conflict affiliation from an uninvolved bystander to the conflict victim) may represent an expression of empathy in which the bystander consoles the victim to alleviate the victim's distress (“consolation”). However, alternative hypotheses for the function of bystander affiliation also exist. Determining whether ravens spontaneously offer consolation to distressed partners may not only help us to understand how animals deal with the costs of aggressive conflict, but may also play an important role in the empathy debate.

Methodology/Principal findings

This study investigates the post-conflict behavior of ravens, applying the predictive framework for the function of bystander affiliation for the first time in a non-ape species. We found weak evidence for reconciliation (post-conflict affiliation between former opponents), but strong evidence for both bystander affiliation and solicited bystander affiliation (post-conflict affiliation from the victim to a bystander). Bystanders involved in both interactions were likely to share a valuable relationship with the victim. Bystander affiliation offered to the victim was more likely to occur after intense conflicts. Renewed aggression was less likely to occur after the victim solicited affiliation from a bystander.

Conclusions/Significance

Our findings suggest that in ravens, bystanders may console victims with whom they share a valuable relationship, thus alleviating the victims' post-conflict distress. Conversely victims may affiliate with bystanders after a conflict in order to reduce the likelihood of renewed aggression. These results stress the importance of relationship quality in determining the occurrence and function of post-conflict interactions, and show that ravens may be sensitive to the emotions of others.

Copyright: © 2010 Fraser, Bugnyar. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This study was funded by the European Science Foundation (COCOR: I-105-G11; http://www.esf.org) and the FWF (Fonds zur Foerderung der wissenschaftlichen Forschung; START: Y366-B17; http://www.fwf.ac.at). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

The article begins with a lengthy introduction to the study of bystander affiliation and consolation in various non-human animals, including chimps, dogs, wolves, and rooks. They then introduce their working hypotheses going into this study with ravens:

Although the vast majority of work on bystander affiliation has been conducted on primates, and in particular on apes, bystander affiliation has recently been demonstrated in a handful of non-primate species, including dogs [33], wolves [34] and rooks [35]. As would be expected on the basis of differences in their social systems, and thus in the quality of their relationships, the patterns of post-conflict behavior across those species vary. Consistent with patterns observed in apes, reconciliation and bystander affiliation occur in dogs and wolves [33], [34], although solicited bystander affiliation was also found in these species while it may be absent in chimpanzees: [27], [36][38]. In contrast, rooks show patterns of post-conflict behavior that differ from any primate species as reconciliation is absent but both bystander affiliation and solicited bystander affiliation occur, although only between pair mates [35].

Here, we investigated the post-conflict behavior of ravens (Corvus corax), another member of the corvid family famed for their primate-like cognitive abilities [39][41] and complex social behavior [42][45]. Ravens are larger than rooks and have a comparatively longer maturation period, not reproducing until at least their third year [46], and occasionally delaying reproduction until as late as their tenth year (T. Bugnyar, unpublished data). Prior to pair-formation and the onset of territorial behavior, ravens form large non-breeder flocks during which time they may experience a broad network of social relationships [47], [48]. Recently, the value, compatibility and security of all dyadic social relationships within our captive population of ravens were ascertained [49]. This information enabled us to take advantage of the extended period during which subadult ravens have a variety of social relationships, and in particular valuable partners outside of the pair bond, to apply the predictive framework for the function of bystander affiliation [30].

As ravens live in much less stable populations than the many primate species in which reconciliation has been demonstrated and as raven sociality is characterized by a high degree of fission-fusion dynamics [50], making dispersal a more feasible and less costly option both before and after aggressive conflict, we predicted that reconciliation was not likely to be widespread and may only occur between those partners who share highly valuable relationships, for whom aggressive conflict is likely to be rare. Furthermore, the risk of renewed aggression between former opponents is likely to be high, making reconciliation too costly to occur. Consolation may thus occur as an alternative distress-alleviating mechanism. In order to find out whether ravens spontaneously provide reassurance to distressed parties, as the term consolation suggests, and to see how affiliation initiated by the bystander differs from affiliation initiated by the victim, we investigated the determinants of bystander affiliation and solicited bystander affiliation, examining in particular at quality of the bystander's relationship with the conflict opponents. We made the following predictions:

  1. If bystander affiliation serves to alleviate the victim's distress (consolation), it is likely to be provided by valuable partners, as these are more likely to be responsive to each other's distress, and may occur after more intense conflicts, when the victim is more likely to be distressed [21], [30]. Solicited bystander affiliation may also alleviate the victim's distress, but empathy is not required.

  2. If bystander affiliation serves a relationship repair function through mediation of a valuable partner, the bystander is likely to share a more valuable relationship with the aggressor than with the victim [25], [30]. Solicited bystander affiliation is unlikely to serve a similar function as the victim may face a high risk of aggression on approaching a bystander who shares a valuable relationship with the aggressor.

  3. Bystander affiliation is predicted to serve a self-protection function if victims redirect aggression towards bystanders and the bystander-victim relationship is characterized by a low degree of compatibility and/or security, as those bystanders are most likely to be at risk of redirected aggression [26], [27], [30]. If solicited bystander affiliation occurs, it cannot fulfill the same function.

  4. Finally, we predicted that if bystander affiliation or solicited bystander affiliation protects the victim from renewed attack from the aggressor, the risk of renewed aggression would be lower following the interaction than in its absence.

When they introduce the study design, it is revealed that the ravens in the study were hand-reared at the Konrad Lorenz Forschungstelle, Austria, after being removed from a zoo next and from the wild.

I'm not a big fan of this, although I can see why it is necessary. It does make me wonder if the ravens are more social as a result of being raised by humans. Likewise, would ravens in the wild be less likely to show support - in this case it could be a case of bonding resulting from being together in captivity. Or maybe the ravens would be more socially oriented if they had been socialized with other wild ravens and not in captivity.

Questions abound after reading the format. Still . . . .

Here is the discussion:

The occurrence of reconciliation could not be confirmed in this group of ravens, consistent with findings in rooks [35]. Reconciliation has been shown to repair the opponents' relationship and reduce post-conflict distress [4], [55], and is thus considered to be the preferred post-conflict interaction in terms of mitigating the costs of aggressive conflict [6]. However, reconciliation should still only occur when its benefits outweigh the costs. Victims were at higher risk of renewed aggression in post-conflict than matched-control periods, suggesting that the risks of renewed aggression upon reconciliation may be too high.

In contrast to reconciliation, both bystander affiliation and solicited bystander affiliation were demonstrated as post-conflict interactions in ravens. Bystander affiliation was more likely to occur after more intense conflicts, which, as victims may experience a higher degree of distress following more intense conflicts, suggests that bystander affiliation may indeed serve a distress-alleviating, or consoling, function. Furthermore, bystanders who provided post-conflict affiliation were likely to share a valuable relationship with the victim of aggression, supportive of a distress-alleviating function as such partners are more likely to be responsive to each other's distress [56], an effect even more likely for kin. Our results are consistent with previous research showing that consolation in chimpanzees is provided by kin and other valuable partners [21], [32].

Sharing a valuable relationship with the victim does not, however, necessarily rule out the possibility that the bystanders also share a valuable relationship with the aggressor, and thus bystanders may still be acting as proxies for the aggressor in reconciling the opponents. For this to be the case bystanders would be expected to share a more valuable relationship with the aggressor than with the victim [25], [30]. Our findings show that bystanders shared more valuable, more compatible and more secure relationships with the conflict victim than with the aggressor, evidence that in ravens opponent relationship repair through mediation of a valuable partner is an unlikely function for bystander affiliation.

The fact that bystanders shared a valuable relationship with the victim, and that their relationship was no less compatible or secure than the victim's relationship with non-affiliating bystanders lead us to reject the hypothesis that bystanders affiliate with the victim of aggression to protect themselves from redirected aggression, as such bystanders are unlikely targets [30]. Furthermore, as redirected aggression could not be demonstrated as a post-conflict interaction, bystander affiliation is unlikely to serve a self-protection function in this group of ravens.

Interestingly, in chimpanzees, the only species in which consolation has been shown, most studies found that solicited bystander affiliation did not occur [27], [36][38], [57]. Conversely, we found not only that solicited bystander affiliation occurs in ravens, but that it is directed towards the same bystanders (valuable partners) who are likely to direct post-conflict affiliation towards victims. Furthermore, when one form of bystander affiliation occurred, the other was also likely to occur. However, the fact that aggression was less likely to occur after solicited bystander affiliation, but not unsolicited bystander affiliation, is suggestive of differing functions for the two interactions. The reduced risk of renewed aggression after solicited bystander affiliation suggests that victims may affiliate with bystanders in order to protect themselves from further attack.

According to the predictive framework, our findings are consistent with a distress-alleviating function for bystander affiliation and should thus be considered to be consolation. The term ‘consolation’, however, infers not only the function of the interaction, alleviating the victim's post-conflict distress, but also its mechanism, empathy for the distressed victim. That bystander affiliation was more likely to occur after intense conflicts, when victims were more likely to be distressed, and that it was most likely to be provided by valuable partners, are supportive of both the functional and mechanistic components of consolation. As emotional contagion (when a subject's emotional state reflects the state perceived in a partner [7], [11]) forms the core basis of empathy, it seems likely that potential consolers would be more likely to respond the perception of increased distress. Moreover, empathy is promoted by close social bonds [11], [58], [59], consistent with our finding that bystander affiliation was provided by bystanders with whom the victim shared a valuable relationship. That kin (a subset of valuable partners) were most likely to console the victim further increases support for ravens' emotional sensitivity to others, as predictions for the occurrence of empathy are consistent with kin selection theory [7].

Whether the initiator of post-conflict affiliation between a bystander and a victim is the bystander or the victim is a critical differentiation when a consoling function is considered because while both interactions may alleviate the victim's distress, only affiliation initiated by the bystander is likely to require empathy. However, if consolation provided by a bystander is preceded by a vocal or other signal from the victim ‘requesting’ support, such a cognitive ability may not be necessary. Thus, although we found suggestive evidence for different functions for bystander affiliation and solicited bystander affiliation, caution must always be taken when interpreting the initiator of an interaction, as signals prior to the first physical interaction may go undetected. Notably, vocalizations were not recorded during this study, and are not usually taken into account in studies of post-conflict behavior (exceptions: [24], [60]), despite the role that they may play in the facilitation of physical affiliative interactions.

All studies on consolation thus far have, for methodological reasons, focused on the effect of consolation on the victim rather than on the consoler. In order to fully understand the mechanism behind consolation, however, we really need to understand more about the consequences of offering consolation for potential consolers. Firstly, although bystanders may experience post-conflict distress [61], we do not know whether consolation alleviates the consoler's as well as the victim's distress. Although empathy may be involved either way, if consolation alleviates the consoler's distress, it may occur as a result of ‘personal distress’, (self-centered distress born from empathy with another's distress [7]) rather than ‘sympathetic concern’ (concern about another's state and attempts to ameliorate this state), which relies on the separation of internally and externally generated emotions. Secondly, if providing consolation entails a risk of aggression for the consoler, the costs of such an act suggest that the consolers' behavior is altruistic. Such ‘directed altruism’ implies an underlying mechanism of sympathetic concern [7]. Although we were not able to analyze the relative increase in risk of aggression that a bystander faces when consoling a victim, in six out of 64 cases of consolation (9.4%), the consoler was subsequently attacked (five times by the aggressor, once by another bystander) within the post-conflict period. In one additional case, a potential consoler (a valuable partner of the victim) was attacked by the aggressor after approaching the victim, but before consolation could take place. It seems likely, therefore, that providing consolation is not risk-free, and may thus be altruistic.

The patterns of post-conflict behavior observed in ravens match what we would expect from what we know about the structure of their relationships. As a pair-bonded species, adult ravens are likely to share valuable relationships primarily with their mates, and thus patterns of post-conflict behavior among adults are expected to resemble those described in rooks [35], where post-conflict bystander affiliation occurs only within pairs and reconciliation is completely absent. However, sub-adult ravens form large non-breeder flocks [47], [48] and actively recruit others to feeding sites [62], conferring a competitive advantage at monopolizable food sources when competing with territorial pairs [63]. Thus, sub-adult ravens may cultivate valuable relationships with a greater number of individuals [49], which may be reflected in their conflict resolution strategies. In this study, patterns of post-conflict behavior suggested that bystanders consoled victims with whom they shared valuable relationships, indicating that the ravens may employ strategies similar to those used by chimpanzees to alleviate distress and mitigate the costs of aggressive conflict. Furthermore, our findings are consistent with the idea that ravens may show similar expressions of empathy for valuable partners. More research is needed to understand the consistency of patterns of raven post-conflict behavior across populations and developmental periods and how transferable such patterns observed in aviary-housed ravens are to wild ravens. Nevertheless the findings of this study represent an important step towards understanding how ravens manage their social relationships and balance the costs of group-living. Furthermore, they suggest that ravens may be responsive to the emotional needs of others.


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