Our results provide the first evidence to suggest that New Caledonian crows have the cognitive capacity to manufacture objects from a mental template. The New Caledonian crows tested here manufactured items that matched the relative size of the previously rewarded templates, without being rewarded for doing so during manufacture test trials and without templates being present at the time of manufacture. One bird in particular, Emma, manufactured pieces that were highly similar to each template, and made secondary modifications to reduce the length of overly large pieces. This strongly suggests that this crow possessed a capacity to remember and reproduce the absolute, not just relative, size of rewarded templates.

Alternative explanations to the crows using mental representations of the different, previously experienced card designs to drive manufacture are ruled out by the design of our study. Crows were not rewarded for manufacturing card of different sizes during training. In fact, crows had only been rewarded for ripping pieces of paper or card irrespective of size during training and so would be predicted to rip pieces of card of any size if they simply transferred learnt rules from training to test. Instead, crows clearly used their prior experience of choosing card of a particular size to then guide subsequent card manufacture, despite no small or large card templates being visible for crows to base manufacture off and the apparatus being identical across conditions. Even during the test, due to us rewarding 50% of card manufacture trials, irrespective of the size made, there was no differential reinforcement that the crows could have used to guide their tool manufacture. Thus, the only way that crows could have made a card template of the correct size was if they had a mental representation of its size, there were simply no physical cues available to guide them.

Our results provide evidence for one of the key predictions of the mental template hypothesis, namely that New Caledonian crows have the cognitive capacity to manufacture items that are similar to previously experienced templates. While there are clearly several other predictions of this hypothesis that require testing, given the results here, we argue that mental template matching is now the leading hypothesis to explain why New Caledonian crow tools show some of the hallmarks of cumulative cultural evolution. Other hypotheses, such as language, teaching, and imitation, can be ruled out due to past work establishing that New Caledonian crows do not have these abilities. In contrast, the mental template matching hypothesis is supported by the results here and recent work showing that humans can iteratively improve on the design of manufactured artefacts such as constructing paper planes18 or baskets to transport rice17, when copying solely the products of social learning, rather than observing an interaction between another social agent and the product. Finally, the mental template matching hypothesis fits well with this species’ ecology. The tendency to acquire basic stick tool manufacture is widespread, develops early, and appears to have a genetic basis in these crows31. In contrast, pandanus tool manufacture is not universal, and, when it does occur, adult-like tool manufacture develops slowly over the first year of life26. During this time, juveniles associate closely with their parents32, regularly borrowing their parents’ tools and using them to acquire food26. Thus, juveniles have ample opportunities to form a mental template of a particular tool design in the wild from both observing and using the tools of their parents. This template allows these crows to recreate this tool even when neither parents nor the parents’ tools are within sight. Crows could then modify this template during their extensive experience of foraging with the tool via differential reinforcement33, leading to the development of tool innovations. Innovations would then be incorporated into the mental template of subsequent generations allowing for the faithful transmission of tool designs with iterative improvements over time. This hypothesis therefore explains the maintenance of different pandanus tools in the wild over decades, in the absence of specific ecological correlates, and the absence of evidence for imitation in this species. Turning to captivity, the behaviour of the New Caledonian crows tested here also bears considerable similarities to one of the most famous instances of tool manufacture by these birds. In 2002, Betty, a captive New Caledonian crow, spontaneously bent a piece of wire into a hook to pull a bucket out of a tube34. Betty had successfully used a pre-made hook to obtain the bucket on a small number of preceding trials; however, in follow-up tasks she did not appear to possess a full causal understanding of hooks35. One explanation for this surprising behaviour is that Betty had formed a mental template of a hooked wire, which she then reproduced.

The mental template matching hypothesis also fits with our current understanding of avian song learning. The acquisition of birdsong comprises a memorisation phase, during which a juvenile acquires a song template from listening to conspecifics, followed by a production phase, during which juveniles adjust their own vocalisations until they match that of the memorised template29. Although some researchers do not include song in discussions of animal culture (see discussion in36) strikingly, song learning – among both birds and cetaceans – is currently the only domain for which there is robust evidence that cumulative cultural evolution does occur among nonhuman animals37,38. That is, changes in songs are demonstrably passed among individuals via learning, and these changes can accumulate over time39,40. New Caledonian crows are vocal learners, displaying cultural call variation in the wild41; thus, these birds possess the neural architecture for memorising and reproducing auditory input42. In light of our findings, we hypothesize that a similar mechanism may potentially enable them to memorise and reproduce material artefacts.

One key prediction of the mental template matching hypothesis is that this ability transmits information about tool design with high fidelity. Here, it is important to note that our arbitrary manufacture task likely underestimated the fidelity with which tool designs could be reproduced by wild crows. First, we supplied birds with a novel material: card. Card does not rip in a wholly predictable manner and is likely to be a more challenging material than pandanus leaves for these crows (particularly juveniles) to manipulate accurately with only their beak and feet. Pandanus leaves, in contrast to paper, rip in straight lines due to the veins that run parallel to their leaf edges, and can be snipped into precisely with the beak. Thus, the properties of pandanus leaves, used in the wild, limit variation in the form the tool can take. This may allow for higher-fidelity transmission of natural tool designs, than we observed using card that does not rip in fixed, straight lines. Second, the designs we provided were arbitrary, and birds were rewarded at random for the items they produced. This design choice was necessary in the current experiment to ensure performance during manufacture test trials could not be explained by trial-and-error learning or operant conditioning; however, in the wild, producing functional tools has high adaptive significance43, as non-functional deviations from a standard design cannot be used to rake in food. Thus, under natural conditions, it is likely that a capacity for mental template matching would be scaffolded by additional mechanisms, including trial-and-error learning, to facilitate the high-fidelity transmission of tool designs44,45. Future work, assessing New Caledonian crow manufacture under conditions that more closely replicate their natural environment is needed to confirm this.

Further research should also consider how long New Caledonian crows’ mental representations persist over time. In our experiment, the delay between reminder trials and manufacturing trials was short, allowing us to confirm that any failures to replicate the templates could not have stemmed from forgetting which template was rewarded. However, in the wild, the delay between using another individual’s tools and manufacturing one’s own is likely to be much greater than the intervals tested here. Understanding more about the nature of these crows’ mental representations – including how this information is stored and for how long – will help us to interpret these birds’ behaviour in the wild.

Whether the cognitive abilities demonstrated here are unique to New Caledonian crows, or are more phylogenetically widespread, is currently unknown. Several species manufacture tools30,46 or perform construction behaviours, such as nest building47, and may have the opportunity to observe or use end-products made by other individuals. Another corvid species, rooks, do not habitually manufacture tools in the wild, but will in captivity48 (as do a small number of other species, such as Goffin cockatoos49), suggesting that the cognitive abilities demonstrated here might also be present in related species. Of particular interest is whether some form of mental template matching might account for the transmission of manufactured tool designs among primates, where debate over the existence of cumulative cultures is ongoing23,50,51.

To date, emulative learning mechanisms – learning from end-results rather than actions – have been considered by many researchers to be insufficient to support cumulative cultural evolution8,13. However, the argument that imitation, teaching and language are the only transmission mechanisms capable of supporting cumulative material cultures may stem in part from the fact that the clearest examples of cumulatively evolved human traditions are cognitively opaque52. That is, they involve products for which construction techniques are difficult to infer simply from viewing the product’s final form53. This is the case for Acheulean stone tools, where a novice cannot infer the precise technique used to strike a core simply from inspecting a finished tool12. However, many situations – including the creation of pandanus tools by New Caledonian crows – are likely to be more cognitively transparent, where manufacture methods can be inferred or discovered without explicit guidance. Here, emulation could be sufficient to enable cultural transmission and evolution. Evidence for this comes from human transmission-chain studies, where end-state emulation can lead to cumulative improvements on cognitively transparent tasks, such as constructing paper planes18 or baskets to transport rice17, but not on cognitively opaque tasks, such as manufacturing stone tools54,55. Prior to the emergence of stone tools, it is likely that hominin tool behaviour involved a greater proportion of cognitively transparent behaviours56, and emulative processes may have played an important role in their transmission17. These findings also raise the possibility that other cases of transparent tool manufacture, such as the varied fishing probes manufactured by chimpanzees50, could potentially allow for cumulative cultural evolution. In sum, our results provide the first demonstration, to our knowledge, that a non-human, tool-making species can manufacture items that match the size of previously rewarded templates. Our findings take the first step towards uncovering why New Caledonian crows show evidence of cumulative cultural evolution. While further work is clearly needed to test other predictions of the mental template matching hypothesis, our results do establish this mechanism as a leading contender for the wild tool designs of this species. A capacity for manufacture via emulation, through a mental template matching mechanism, could potentially reflect one of the minimal cognitive requirements for the emergence of cumulative material cultures.