New Caledonian crows reason about hidden causal agents

Imagine a bird looking down on a monkey moving through a forest canopy. Generally, the bird will be able to observe both the monkey moving and the canopy shaking at the same time. Sometimes, however, when the canopy is thick overhead, the bird may only observe that, against a background of stationery leaves, there are waves of moving leaves that can start and stop abruptly. Humans are able to imagine why the leaves are moving when the monkey is out of sight. They can hypothesize that there is a hidden causal agent that must be moving the leaves because when the wind is not blowing, the canopy does not shake on its own. We make such inferences from a very early age. Between 7–10 mo of age, infants begin to show surprise if a bean bag is thrown from behind a screen and the screen is then lifted to show an inert object, rather than a causal agent such as a hand (1, 2). The use of such causal reasoning underpins not only scientific (3) and religious thought (4, 5) but also our sophisticated tool-using abilities (6) and understanding of social interactions (7–9). However, we currently have little idea how such cognition evolved.

One way to increase our knowledge would be to study the evolution of this type of causal reasoning in other species. Unfortunately, there is no evidence to date that any nonhuman animal has the ability to make inferences about hidden causal mechanisms (10–14). However, no studies have attempted to recreate ecological situations, such as the canopy problem outlined above, where the ability to make inferences about hidden causal agents would be highly adaptive. To solve the canopy problem an animal must infer the presence of a hidden causal agent from the movement of an inanimate object. We presented eight New Caledonian crows, a species that has produced behavior suggestive of complex causal cognition (15–23), with the hidden causal agent (HCA) problem. This experimental paradigm mirrored the canopy problem by creating a situation where an animal had to infer what caused an inanimate object to move. The crows were first given experience extracting food with a tool from a box. The box was then placed close to a novel hide that had been setup in the crows’ aviary. The entrance to the box faced the hide, so crows had to turn their heads directly away from the hide to pull the food out of the tube with the tool. Testing began once the crows were able to extract the food when the box was 20 cm from the hide. The crows were first given three trials of the hidden causal agent (HCA) condition. Here, they observed two humans walk into the aviary. One, the agent, walked into the hide and so became hidden from the crows. A wooden stick was then probed in and out of a hole in the hide wall 15 times toward the baited hole. The agent then exited the hide and left the room. At this point the second human, who had stood 1.5 m from the hide in the corner of the room with closed eyes and hands held in front of the body, also left the room. The crow was now free to come down to the table, pick up a tool, and use it to extract the food from the box. The crows were then given three trials of the unknown causal agent (UCA) condition. Here, one human entered the cage and stood in the far corner, with closed eyes and hands held in front of the body as before. The tool was then probed through the hole in the hide 15 times. The human then left, and the crows again were free to come down to extract food. In both the HCA and UCA conditions, the stick moved in the same way because it was actually moved by an experimenter pulling on a string that could be pulled either from within the hide or from outside the testing room.

The movement of the probing stick was a novel stimulus and, thus, likely to elicit neophobic responses from the crows. The movement of the stick was also likely to be an aversive stimulus for the crows as it moved into the space where the crows would put their heads when they attempted to extract the food from the box. When the crows used a tool in the hole, they had to face away from the hide and, thus, could not easily monitor whether the stick was being moved. Thus, a repetition of the sticks’ movement was likely to result in the stick hitting the crows in the back of the head. (Of course, in reality, there was no chance of the stick hitting the crows because the experimenter never pulled the string when the crows were on the table.) For the crows to extract food in this situation, they needed to minimize the perceived risk of being hit by the stick emerging from the hide during tool use. There were two potential ways they could do this. First, they could be very cautious after seeing this stick being probed for the first time. The level of caution would then be progressively reduced each time the crows used a tool in the box and the stick did not appear. That is, the crows would initially show a neophobic response and then gradually habituate (24, 25). An alternative way for the crows to minimize risk would be for the crows to predict the stick’s movement by reasoning about why the stick was moving. In the first condition, the crows observed the human enter the hide, the stick move, and the human leave both the hide and cage. If the crows could attribute the stick’s movement to the hidden human, they could infer that when the human left the room, the stick would not move again. In contrast, in the second, unknown condition, if the crows were capable of causal reasoning, they would predict that the stick might move again because they had not observed a potential causal agent leave the hide. This “causal reasoning hypothesis,” therefore, made the opposite prediction from the “habituation hypothesis” outlined above. In the hidden agent condition, the crows should show similar levels of caution to those in the final trial of habituation to the hide. In the unknown condition, the crows should show a high level of caution, despite the movement of the stick no longer being a novel stimulus.

To test between these hypotheses, we measured the degree of caution in the crows’ behavior. We examined the number of times the crows both inspected the hide and abandoned probing across our experiment. Hide inspections were defined as a crow orientating its head toward the hole and then moving its head toward the hide, so that one or both eyes was/were in line with the hide. Orientations to the hide were not scored if the crow was not first looking toward the baited hole or if the crow looked at an area of the cage other than the hide after looking at the hole. An abandoned probe was defined as a crow inserting the tool into the hole and then leaving the testing area without extracting the food.