We provide evidence that pet dogs distinguish between human true beliefs & false beliefs scenarios, suggesting that the mechanisms underlying sensitivity to others' beliefs have not evolved uniquely in the primate lineage

Dogs follow human misleading suggestions more often when the informant has a false belief. Lucrezia Lonardo, Christoph J. Völter, Claus Lamm and Ludwig Huber. Proceedings of the Royal Society B: Biological Sciences, July 21 2021. https://doi.org/10.1098/rspb.2021.0906

Abstract: We investigated whether dogs (Canis familiaris) distinguish between human true (TB) and false beliefs (FB). In three experiments with a pre-registered change of location task, dogs (n = 260) could retrieve food from one of two opaque buckets after witnessing a misleading suggestion by a human informant (the ‘communicator’) who held either a TB or a FB about the location of food. Dogs in both the TB and FB group witnessed the initial hiding of food, its subsequent displacement by a second experimenter, and finally, the misleading suggestion to the empty bucket by the communicator. On average, dogs chose the suggested container significantly more often in the FB group than in the TB group and hence were sensitive to the experimental manipulation. Terriers were the only group of breeds that behaved like human infants and apes tested in previous studies with a similar paradigm, by following the communicator's suggestion more often in the TB than in the FB group. We discuss the results in terms of processing of goals and beliefs. Overall, we provide evidence that pet dogs distinguish between TB and FB scenarios, suggesting that the mechanisms underlying sensitivity to others' beliefs have not evolved uniquely in the primate lineage.

4. Discussion

This study aimed at investigating whether dogs would spontaneously behave in a different way in response to a misleading suggestion from a human informant with a TB or a FB and this is indeed what we found in experiment 1. The combined results of experiments 1 and 2 suggest that retroactive interference is not a likely explanation for the behaviour of dogs in this task. Finally, the results of experiment 3 show that performance in this task is subject to breed (group) differences.

Both conditions of experiment 1 (TB and FB) were characterized by very similar behavioural cues: the hider always moved food from container A to container B; the communicator always left and re-entered the room after the same amount of time, and afterwards always suggested the empty container A. Hence, the only difference between the TB and FB condition in experiment 1 was the moment in which the communicator re-entered the room: before (TB) or after (FB) the food displacement by the hider. From this difference, it could be inferred whether the communicator could or could not see the displacement of food and hence whether she was left with a FB (that food was still in bucket A), or whether her belief (that food was in bucket B) was updated and veridical.

In the absence of any previous training, dogs in the two groups of experiment 1 (TB, FB) behaved differently in response to the same misleading suggestion. More dogs in the FB than in the TB group approached and touched the suggested (empty) container. Given that the two scenarios differed in the timing of the communicator re-entering the room, we introduced a third condition to rule out the possible influence of the moment of re-entry. Indeed, one could have argued that dogs in the FB group of experiment 1 might have been distracted by the salient event of the communicator re-entering the room after the final hiding of food and hence were more inclined to trust the human signal due to retroactive interference (as already proposed for FB studies with human infants and adults [20,49]).

The events in the CTB condition had the potential to elicit the same retroactive interference (if not more) as those in the FB scenario. Indeed, dogs in the CTB witnessed the communicator both leaving and re-entering the room after the final hiding of food. The combined results of experiments 1 and 2, however, show that dogs in the two true belief scenarios reacted in the same way despite the difference in the order of the events. Therefore, dogs' responses did not depend on subtle details of the sequence of events in the experimental procedure. In line with findings that dogs showed an ability to judge human informants on the basis of what these have seen or not [40], our findings thus add further evidence that dogs possess the ability to differentiate between human knowledge states.

Prior to running the experiments, we had predicted that more dogs from the true belief group should have followed the communicator's cue. Surprisingly, instead, more dogs followed the communicator's misleading suggestion when the latter was absent during the food displacement (FB group). Thus, their behaviour was opposite to that of Buttelmann et al.'s human infants and apes [17,41], and to our own pre-registered hypothesis. A possible explanation for this behavioural pattern might reside in the way the communicator's intention was interpreted. In our experiment, the communicator first (during the familiarization trials) proved to be a reliable helper for the dogs and then during the test suggested for the first time the wrong container. In Buttelmann et al.'s studies [17,41], the participants were the ones asked to help the experimenter retrieve a hidden object, which was of no value for the participants themselves. In this kind of helping paradigm, the experimenter's goal was not to communicate to participants the location of the hidden object, therefore it is unlikely that participants viewed the experimenter as untrustworthy. In our task, however, it is possible that dogs in the true belief group interpreted the communicator's misleading behaviour as deceitful, or driven by another (unknown) intention, and therefore more dogs in this group (TB) than in the FB group ignored her suggestion and chose bucket B.

Previous studies have shown that dogs do not follow human misleading pointing gestures blindly (although sometimes they find them difficult to ignore [50]); instead, they can adjust their behaviour flexibly depending on the trustworthiness of the informant [51] and can discriminate between helpful and uncooperative experimenters [52]. Along this line of argument, it seems plausible to assume that dogs in both groups remembered the final location of food (bucket B). However, the communicator's misleading suggestion in the TB scenario might have appeared as deceitful if dogs attributed a true belief to the communicator. Whereas the same misleading suggestion (of bucket A) might have appeared as a mistake ‘in good will’ in the FB scenario if dogs understood that the communicator lacked the relevant knowledge (ignorance) or that she believed food was actually in container A (FB). This might explain why more dogs in the FB than in the TB group followed the misleading suggestion. Indeed, previous research indicates that dogs readily conform to a familiar and unfamiliar human's influence in object-choice tasks even when there is no apparent need to do so and, crucially, even when conforming leads to a suboptimal outcome for the dog [45,53–57]. In particular, Prato-Previde et al. [53] found that younger dogs were more easily misled by a human's influence than older ones, similar to the age effect revealed when pooling experiments 1 and 2 in the current study. We decided to test dogs from five months of age because Barnard et al. [55] had shown that the tendency to conform to human misleading suggestions is present in puppies already at 4 months. Similarly to what happened in our setting, Topál et al. [44] found that dogs in a hiding-finding game kept searching for a toy in previous hiding locations they knew to be empty. The authors suggest that such a ‘rule-following’ behaviour might minimize social conflicts and enhance social cohesion with humans [26,58]. In our task, the communicator with a FB might have been perceived as a mistaken informant who was still playing the game by the same rules as in the familiarization. Instead, the communicator with a true belief (suddenly switching to uncooperativeness) might have been perceived as less trustworthy or violating the rules of the game and this might explain why her suggestion was ignored more often.

Although we did not predict nor pre-register substantial breed effects, we had decided to test only pure-bred dogs in order to be able to explore possible differences. This resulted in the finding that the behaviour of terriers deviated from the one of most other breed groups (electronic supplementary material, figure S2 and S6). In particular, already in experiment 1, we observed a difference in the choice pattern of terriers (FCI group 3), on the one hand, and other breed groups, such as FCI group 2 (in our sample, Schnauzers, Molossoids and Swiss Mountain and Cattledogs), FCI group 7 (pointing dogs) and FCI group 8 (in our sample, retrievers) on the other hand. Unlike other breeds, more terriers from the TB group than from the FB group chose the empty container.

To confirm this unpredicted result, we tested new cohorts of terriers and border collies in experiment 3. We replicated our initial findings: while border collies behaved in accordance with the majority of breeds in experiment 1 (although we did not find a statistically significant difference between conditions; for comparison, the performance of the border collies in experiment 1 is shown in electronic supplementary material, figure S2) terriers exhibited the opposite behavioural pattern. The response pattern of the latter FCI group matches our initial prediction and is consistent with human infants' and great apes’ performance in a similar task [17,41].

We can only speculate about the reasons for the observed differences between FCI groups. The breed differences that have been reported in a scientific context mainly concern specific temperament traits [59,60], behaviours [61–63] and interspecific communicative abilities (e.g. tendency to look at a human's face and to follow pointing gestures [64–66]). Based on the working history of some breeds, Gácsi et al. [64] classified dogs into two main categories: cooperative and independent workers. Accordingly, dogs in the first category have been selected for cooperating while keeping continuous visual contact with their human partner, whereas the latter have been selected for working without any human visual contact. The authors found that cooperative workers (e.g. shepherds and gundogs) were more willing than independent ones (e.g. terriers, hounds, greyhounds and sledge dogs) to follow human distal, temporary pointing gestures. However, only limited attention has been devoted to the empirical investigation of dog breed differences in cognition [67]. An interesting exception is the study by Heberlein et al. [68], who found that independent workers and family dogs, when forbidden to eat food, were more skilled at taking their owner's perspective than cooperative workers. Based on the results of experiment 1, we decided to compare dogs considered as cooperative workers (here: border collies) to independent workers (here: terriers) in experiment 3. Terriers were chosen because they had shown the initially hypothesized response pattern in experiment 1; border collies because they have been extensively tested in studies on social cognition in our and other laboratories [69–71].

In the current study, breed differences might be indicative of different interpretations of the intentions behind human communicative signals. Indeed, terriers were not only more independent of the communicators' signal irrespective of condition, but they also reacted in the opposite way to the scenarios compared to pointing dogs, retrievers, molossoids and border collies (electronic supplementary material, figure S2 and S6). In particular, it is possible that many of the ‘cooperative workers’ in our study interpreted the communicators' cue in the TB scenario as deceitful while many terriers interpreted it as motivated by the intention to show something new. Marshall-Pescini et al. [45] suggested that the intentions behind human actions might play an important role in causing dogs’ social bias (i.e. the tendency to make counterproductive choices under the influence of human signalling). From our findings, it seems possible that artificial selection made cooperative workers more skilled at detecting human deception relative to independent workers. Indeed, it has been suggested that one of the necessary conditions for the emergence of reciprocal altruism is that the cooperating animals need to be able to recognize cheaters [72]. However, to test this hypothesis, future research is needed to target specifically the reaction of a larger sample of other ‘independent workers' (e.g. sled dogs, hounds and greyhounds) to this task.

The evolutionary origin of dogs' ability to distinguish between TB and FB of humans remains an open question. Future studies should examine how dogs and wolves (Canis lupus) compare in the current paradigm. If dogs’ increased attention to human mental states results from the process of domestication, wolves are not likely to perform similarly to dogs. Additionally, future research should clarify based on broader phylogenetic comparisons (e.g. comparing dogs with other domesticated species or primate species) whether identical or only superficially similar mechanisms have evolved across species and taxa.

In conclusion, our study provides the first experimental evidence that dogs distinguish between a TB and a FB condition in a change-of-location task. Although in both conditions the communicator suggested the empty container, different numbers of dogs in the two groups followed this cue. For most dog breeds, this response pattern was in contrast to those found in human infants and great apes—with the notable exception of the terrier breed group. This raises the possibility that pet dogs attribute to human informants, in the absence of any training, not only different knowledge states, but also different intentions and beliefs. Distraction [20] is very unlikely to account for this finding. Indeed, not only the good performance in the familiarization phase but also the fact that the majority of dogs in experiment 1 (61.5%) and in the CTB group (72%) followed their own knowledge proved that the dogs were sufficiently attentive to find food hidden and displaced.

Based on the experience dogs made during the familiarization phase that the communicator's suggestion was trustworthy, the cueing of the empty container in the test has likely caused a conflicting information for the dogs. A possible account for the difference between FB and TB groups in dealing with this misleading suggestion by the human informant is in terms of mental state attribution. In the FB group, a decent number of dogs from cooperative breeds might have followed the wrong suggestion of the informant by attributing to her a FB and consequently a ‘justified’ mistake in good will. However, in the TB groups, a lower number of dogs followed the same suggestion because this appeared deceitful or at least unjustified based on the informant's epistemic state. By contrast, dogs from more independent breeds like terriers may have interpreted the TB informant's suggestion as invitation to explore the first hiding place further and therefore relatively more terriers of the TB group followed it. Of course, such mentalistic accounts in terms of how the situation appears from the communicator's perspective and what the intention of the communicator is when suggesting the wrong container, would need additional evidence from experiments with specific controls for other accounts (behavioural rules, ignorance, submentalizing, minimalist accounts, experiential record-keeping and awareness relations; see [6,18,20,49]). Until that, the possibility that dogs possess what seems at least an implicit FB understanding remains an exciting hypothesis.