Tuesday, 25 July 2017

Ravens remember people who suckered them into an unfair deal
No one likes a con artist. People avoid dealing with characters who have swindled them in the past, and—according to new research—birds avoid those people, too. Ravens, known more for their intelligence, but only slightly less for their love of cheese, were trained by researchers to trade a crust of bread for a morsel of cheese with human partners. When the birds then tried to broker a trade with “fair” and “unfair” partners—some completed the trade as expected, but others took the raven’s bread and kept (and ate) the cheese—the ravens avoided the tricksters in separate trials a month later. This suggests that ravens can not only differentiate between “fair” and “unfair” individuals, but they retain that ability for at least a month, the researchers write this month in Animal Behavior. Ravens have a complex social life involving friendships and rivalries. Their ability to recognize and punish dishonest individuals, even after a single encounter, may help explain how cooperation evolved in this group of birds. For people, though, the moral of the story is simple: Be nice to ravens.
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DOI: 10.1126/science.aan6931

Katie Langin

Animal Behaviour

Volume 128, June 2017, Pages 69-78
Animal Behaviour

Ravens remember the nature of a single reciprocal interaction sequence over 2 days and even after a month

Under a Creative Commons license
open access


Ravens can remember whether experimenters were fair or not in an exchange paradigm.
They prefer exchanging with experimenters that were fair to them previously.
This memory can last 2 days to even a month.
Birds that observe such exchanges do not seem to remember.
Experience with the paradigm helps observing birds to remember who is fair.
To explain reciprocity, direct or indirect, several proximate mechanisms have been proposed, yet little attention has been given to the specific underlying cognitive mechanisms. Regardless of what proximate rules underlie reciprocity, some kind of memory would be paramount. Corvids in general, and ravens, Corvus corax, specifically, have been shown to possess an array of sophisticated cognitive mechanisms involved in memory. In this study, we tested the memory of nine ravens in an exchange paradigm where they could exchange a low-quality for a high-quality food item. Specifically, we tested whether they remembered who was a reliable ‘fair’ experimenter and who would not reliably exchange (the ‘unfair’ experimenter), and whether they would subsequently choose to interact with the former when given the choice. In addition, we tested whether ravens that observed the initial seeding of information about who was ‘fair’ or ‘unfair’ could transform bystander information into first-person interactions, i.e. also preferring to interact with the ‘fair’ experimenter when given the choice. The results show that ravens with first-hand experience were more likely to interact with experimenters with whom they had had a positive previous experience, and that this memory lasted at least 1 month. In contrast, observers did not distinguish between the experimenters when given the choice to interact with them. Previous first-hand experience with the paradigm, however, seemed to help observers to be more successful in solving the task, albeit not significantly above chance. In sum, this study shows memory for direct reciprocity in ravens, and tentatively suggests memory for indirect reciprocity. Accordingly, these results provide hints for the underlying mechanism of memory in raven social interactions.


animal memory
common ravens
exchange paradigm
indirect reciprocity
Reciprocal altruism (Trivers, 1971) has proven a powerful theory explaining the evolution of repeated prosocial interactions between individuals. In such repeated interactions individuals may exchange different goods and commodities with each other (Hemelrijk & Ek, 1991; Kappeler & van Schaik, 2006; Sachs, Mueller, Wilcox, & Bull, 2004). For example, there is ample evidence that primates exchange grooming (meta-analyses on 22 primate species: Schino & Aureli, 2008), as well as agonistic support in conflicts (Schino, 2007; Smith et al., 2010), and that they interchange both commodities (meta-analysis on 14 primate species: Schino, 2007). A similar picture has recently started to emerge in birds such as corvids that form long-term social bonds (Emery, Seed, von Bayern, & Clayton, 2007). Ravens, Corvus corax, for instance, were found to exchange coalitionary support among each other as well as interchanging the avian equivalent of grooming (preening) for support, and do so most with those individuals with whom they share a bonded relationship (Fraser & Bugnyar, 2010, 2012). Moreover, ravens have been shown to stop cooperating when their partner cheats (Massen, Ritter, & Bugnyar, 2015). Both rooks, Corvus frugilegus, and ravens cooperate better with affiliates (Seed, Clayton, & Emery, 2008), and ravens even actively choose to cooperate with friends when given a choice between different partners (Asakawa-Haas, Schiestl, Bugnyar, & Massen, 2016).
Several hypotheses have been proposed for the underlying proximate mechanisms of reciprocation. Calculated reciprocity refers to the active scorekeeping of the value and amount of what has been given and received (de Waal & Luttrell, 1988), a mechanism so far only shown in orang-utans, Pongo abelii (Dufour, Pelé, Neumann, Thierry, & Call, 2009). Attitudinal reciprocity, which was shown in capuchin monkeys, Cebus apella (de Waal, 2000), describes a mechanism in which the choice to cooperate depends on the attitude the interaction partner has recently shown towards the subject (Brosnan & de Waal, 2002; de Waal, 2000). Emotionally mediated reciprocity is related, but stresses the emotions derived from a long-term series of interactions and has been investigated by studying the time frame of the reciprocal exchange of grooming and agonistic support in Japanese macaques, Macaca fuscata (Schino, Polizzi di Sorrentino, & Tiddi, 2007). Finally, symmetry-based reciprocity suggests that the initiation and maintenance of reciprocal relations is solely based on the symmetrical features of two individuals (de Waal & Luttrell, 1988). Brosnan and de Waal (2002) argued that many examples of animal altruism might depend on symmetry-based reciprocity (e.g. Wilkinson, 1984, 1988). However, a recent modelling study revealed that this is not an evolutionarily stable strategy to maintain reciprocity in a group (Campennì & Schino, 2016). In addition to direct forms of reciprocation, there is indirect reciprocity, where A helps B because B has the reputation of being cooperative, as A observed B helping C in the past (Nowak & Sigmund, 2005). This has, for example, been shown in dogs, Canis lupus familiaris (Chijiiwa, Kuroshima, Hori, Anderson, & Fujita, 2015), capuchin monkeys (Anderson, Kuroshima, Takimoto, & Fujita, 2013) and squirrel monkeys, Saimiri sciureus (Anderson, Bucher, Kuroshima, & Fujita, 2016). In contrast, in generalized or upstream reciprocity receiving something leads to a good ‘feeling’ which in turn creates a higher propensity to give something to a third party (Boyd & Richerson, 1989; Nowak & Roch, 2007), which has, for example, been shown in rats, Rattus norvegicus (Rutte & Taborsky, 2007).
Calculated reciprocity, as an example, has been considered cognitively too demanding for nonhuman species (Schino & Aureli, 2010; Stevens & Hauser, 2004; but see Dufour et al., 2009). However, little attention has been given to those cognitive skills that nonhuman animals purportedly lack for the different forms of reciprocity. Some emphasis has been put on the time frame of reciprocation to distinguish attitudinal from emotional systems (Schino et al., 2007), but it does not pinpoint specific traits. Apart from symmetry-based reciprocity and generalized reciprocity, however, all proposed mechanisms rely on some sort of memory, and more specifically on memories of what happened to you in an interaction with a specific individual, or in the indirect case, of interactions between others. Therefore, the aims of this study were to analyse whether ravens can remember (1) who acted cooperatively or defectively in a single session, and (2) an experience of third-party interactions of cooperation or defection. The required memories may rely on numerous cognitive systems working in concert, and it has previously been shown that corvids have several of these systems.
A central memory skill for reciprocity is the recall of someone's identity. Face recognition is an integral part of such recollection. The ability to recognize faces is a conserved skill, found not only in mammals, such as primates and sheep (Tate, Fischer, Leigh, & Kendrick, 2006), but, for example, also in American crows, Corvus brachyrhynchos (Marzluff, Walls, Cornell, Withey, & Craig, 2010) and honeybees, Apis mellifera (Dyer, Neumeyer, & Chittka, 2005). Naturally, interspecies face recognition does not rely on specific predispositions for recognizing faces of members of other species. Rather, much of the recognition results from configural processing of the elements from which a face is constructed, which is a process used by bees as well as humans (Avarguès-Weber, Portelli, Benard, Dyer, & Giurfa, 2010). Face recognition does not suffice, however, if one must remember the cooperativeness of an individual. At the very least, one needs positive or negative emotions associated with the identity. American crows have been shown to make such emotional associations in identity recognition, using neurobiological mechanisms similar to those of mammals (Marzluff, Miyaoka, Minoshima, & Cross, 2012). It has further been shown that ravens can remember the valence of their relationship with conspecifics over years and respond to their calls accordingly (Boeckle & Bugnyar, 2012).
Remembering single events of reciprocal interactions would, arguably, contribute substantially to more economical behaviour in future interactions between the same individuals. There is evidence that large-billed crows, Corvus macrorhynchos, remember the dominance status of another individual, in relation to themselves, after single event interactions (Izawa & Watanabe, 2008; Nishizawa, Izawa, & Watanabe, 2011). It has also been shown that American crows will remember the face of a dangerous human (a trapper of crows) for several years after only one interaction (Marzluff et al., 2010). Moreover, ravens and western scrub jays, Aphelocoma californica, remember which of their group mates was watching them during a single caching event (Bugnyar, 2011; Dally, Emery, & Clayton, 2006).
Memories of single events are often attributed to the workings of an episodic memory system. Episodic-like memories have been exhibited, in relation to different caching contexts, by western scrub jays (for a review see de Kort, Dickinson, & Clayton, 2005). However, so-called one-shot learning in animals is an ill-understood and debated phenomenon (Osvath, 2015). Nevertheless, some studies have provided evidence that chimpanzees, Pan troglodytes, orang-utans and humans share some core features of their memory systems to recall personal experiences from the past (Martin-Ordas, Berntsen, & Call, 2013). Single event learning can, however, be supported by different mechanisms; for example innate defence behaviours and so-called preparedness (Bolles, 1970; Seligman, 1971). The above examples of single event memories in corvids are related either to dominance, fear or caching contexts, domains of great importance for corvids. Regardless of the specific mechanisms underlying their memories, however, we wanted to investigate whether ravens can extend this single-event-memory skill to reciprocal interactions.
Finally, we also wanted to investigate whether ravens can remember and act upon a single interaction sequence of third-party interactions. Indirect reciprocity is generally regarded as cognitively more demanding than direct reciprocity (Nowak & Sigmund, 2005). Among other things, one must be able to form memories of interactions between others, and attribute valence to the actions. However, it has been shown that ravens are capable of representing and remembering the relationships between others, without even having interacted with any of the observed individuals (Massen, Pašukonis, Schmidt, & Bugnyar, 2014), and they also seem to keep track of such third-party relationships over time (Massen, Szipl, Spreafico, & Bugnyar, 2014) suggesting at least some sort of third-party knowledge and memory. Given such extraordinary capabilities in corvids in general and ravens in particular, one could hypothesize that many reciprocal behaviours in corvids also rely on elaborate memory systems. Therefore, we predicted that ravens are able to remember the identity of certain experimenters and their characteristic behaviour (cooperate, defect), and that they prefer interacting with the ‘fair’ experimenter when given the choice at a later stage. Moreover, we predicted ravens would have third-person event memory, expressed by a transfer to a first-person interaction. Consequently, observing birds should show the same behaviour (preference) and exchange rates as the first-hand experienced birds when given the choice at a later test phase. Finally, given the complex fission–fusion dynamics in raven nonbreeding flocks (Loretto, Reimannf, Schuster, Graulich, & Bugnyar, 2016; Loretto, Schuster, & Bugnyar, 2016) that allow for long-term separations of known conspecifics, we predicted that these memories could also last a long time, i.e. from 2 days to a month.