Inhibitory control i.e. blocking an impulsive or prepotent response in favour of a more appropriate alternative, has been suggested to play an important role in cooperative behaviour. Interestingly, while dogs and wolves show a similar social organization, they differ in their intraspecific cooperation tendencies in that wolves rely more heavily on group coordination in regard to hunting and pup-rearing compared to dogs. Hence, based on the ‘canine cooperation’ hypothesis wolves should show better inhibitory control than dogs. On the other hand, through the domestication process, dogs may have been selected for cooperative tendencies towards humans and/or a less reactive temperament, which may in turn have affected their inhibitory control abilities. Hence, based on the latter hypothesis, we would expect dogs to show a higher performance in tasks requiring inhibitory control. To test the predictive value of these alternative hypotheses, in the current study two tasks; the ‘cylinder task’ and the ‘detour task’, which are designed to assess inhibitory control, were used to evaluate the performance of identically raised pack dogs and wolves. Results from the cylinder task showed a significantly poorer performance in wolves than identically-raised pack dogs (and showed that pack-dogs performed similarly to pet dogs with different training experiences), however contrary results emerged in the detour task, with wolves showing a shorter latency to success and less perseverative behaviour at the fence. Results are discussed in relation to previous studies using these paradigms and in terms of the validity of these two methods in assessing inhibitory control.

Funding: The project is financially supported by Austrian Science Fund (FWF) project P21244-B17. Sarah Marshall-Pescini and Friederike Range were supported by funding from the European Research Council under the European Union's Seventh Framework Programme (FP/2007-2013)/ERC Grant Agreement n. [311870] and Zsófia Virányi from the WWTF project CS11-026. The authors further thank many private sponsors including Royal Canin for financial support and the Game Park Ernstbrunn for hosting the Wolf Science Center. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Inhibitory control entails blocking an impulsive or prepotent response in favour of a more appropriate alternative when it is advantageous to do so. Inhibitory control mechanisms can help animals enhance their behavioural flexibility, increasing their adaptive success and this may be especially true in unstable or rapidly changing environments, since in these contexts a once advantageous behaviour can quickly become useless or even counterproductive.

Social environments are in many cases unstable since they are made up of social partners and thus require constant negotiation between individual needs whilst maintaining social relationships such that the individual can continue to benefit from inclusion in the group. These challenges may have driven the selection for increased behavioural inhibition as well as other cognitive processes [1–5].

In the context of food competition amongst conspecifics for example, a subordinate may need to inhibit its prepotent response to access resources in order to avoid aggression from higher-ranking individuals and indeed there is some evidence that species with a steeper and more rigid hierarchical organization may have an increased capacity for inhibitory control [6,7]. Further evidence for a link between social factors and behavioural inhibition comes from a study in which primates with a more complex fission-fusion social structure appear to show an increased capacity for inhibitory control over a range of tests [8].

However, fission-fusion is only one of a number of variables characterizing the potential complexity of a species' social structure. A species’ reliance on cooperation in terms of coordinated actions during hunting and/or pair-bonding and communal pup-raising may be another of these variables, since coordinated actions would require inhibitory control to allow for each individual to take into account the behaviour of the other.

In regards to the potential cognitive mechanisms involved in group hunting, in a recent study, authors suggest that an ability to know when to ‘hold back’ vs. when to join, especially when excited may be an important skill that can affect the success of a group hunt (pp.7) [9]. Indeed the timing of actions (or synchronisation) appears to be the main ability required to achieve a ‘collaborative’ hunt as opposed to a hunt in which each individual is striving to obtain the prey at the same time but with no coordinated action.

Pair bonding has also been suggested to have affected a number of cognitive mechanisms with mixed support from experimental studies. In ungulates, carnivores, bats and birds brain size appears to be associated principally with pair-bonding [10], leading authors to suggest that this type of social organization may be associated with complex cognitive skills based on the need to coordinate and synchronize behaviour (pp. 566) [3]. Similarly van Schaik and colleagues [11–13] conclude that pair-bonding and communal pup-raising is indeed associated with a higher performance in socio-cognitive tasks involving (amongst others) the ability to coordinate actions spatially and temporally (e.g. cooperative problem solving). However, based on the current data it is still not clear whether pair-bonding and communal pup-raising positively affect inhibitory control [12].

In terms of their socio-behavioural ecology wolves and free-ranging dogs show similar social organizations in that they can both live in packs and exhibit differential social relationships between members [14–16]. However, the two species appear to differ in their intraspecific cooperation tendencies: in fact although both wolves and dogs rely on close action coordination with pack members when defending their territories [14,17,18], wolves also rely on group coordination when hunting large game [19] whereas reports of group hunting in free-ranging dogs are rare [20] (but see [21]). Furthermore, wolves show pair-bonding and communal raising of pups, with both members of the pair caring for the young and ‘helpers’ (usually offspring from previous years) often staying behind to assist with raising [14, 17]. Female free-ranging dogs, on the other hand, mostly raise their pups alone [22, 23] or in some rare occasions with the help of the male who typically defends but rarely feeds the pups [24]. Hence, based on the limited information we have on the intraspecific socio-behavioural ecology of the two species, one would predict that wolves should show better inhibitory control than dogs.

However, an alternative hypothesis is that through the domestication process, dogs may have been inadvertently selected for a less reactive, "tamer" temperament (‘the emotional reactivity hypothesis’ [25–27]). Indeed ‘the synergistic hypothesis’ of domestication explicitly proposes that compared to wolves, dogs may show superior abilities in certain communicative tasks with humans (e.g. the pointing task) due to the fact that they are more inclined to inhibit their immediate reactions in favour of delayed rewards [28]. Hence, based on these domestication hypotheses, we would expect dogs to have higher inhibitory control than wolves. It is of course possible that both cooperation and domestication have affected inhibitory control, in which case we would expect both species to show an equally developed capacity for inhibition. If this were the case, one could test a third ‘control species’ closely related to dogs and wolves, but with no history of domestication and less dependent on cooperative activities (such as group hunting) to tease these effects apart. Since canids show a high variability regarding socio-ecological variables that may affect cognitive processes such as behavioural inhibition, they are a great model species to investigate such questions. For example, coyotes and jackals rely less on group hunting than grey wolves and Ethiopian wolves tend to be mostly solitary hunters [29].

In the current study, we contribute to such a comparative analysis of inhibitory control in Canids by comparing the performance of identically raised and kept, pack-living wolves and dogs in two inhibitory control tasks. One of these tasks, the cylinder task has already been used to investigate the inhibitory control ability of 36 species, amongst which dogs, wolves and coyotes were tested [30, 31]. Additionally, we presented our subjects with the fence detour task in which pet dogs and dingoes have been tested so far [32–36]. The animals in those studies, however, have been raised under different conditions and had different learning opportunities. Consequently, it is rather difficult to argue for purely evolutionary causes to explain potential differences in results between them, since arguably, training experience may be one of the more influential variables in the development of inhibition. Accordingly, in order to elucidate to what extent inhibitory control is affected by learning and training experiences in wolves and dogs, we furthermore compared the performance of our pack dogs with groups of pet dogs differing in their training experience. Hence the cylinder task was presented also to groups of trained and untrained pet dogs matched for breed and age, and to a group of pet dogs who were given the cylinder test with no prior training trials, to assess whether the initial learning in this phase may affect performance in the test. The performance of wolves on the cylinder task was hence compared to that of dogs living at the Wolf Science Center (WSC) but also to pet dogs with different experiences, whereas performance on the detour task was compared to results of prior studies using this paradigm [32–36].