In their natural environment, animals face a variety of ecological and social challenges. Theories of cognitive evolution suggest that these challenges have favoured the emergence of cognitive skills that allow individuals to better cope with the problems they encounter in their ecological niches [1, 2]. One of the most basic cognitive skills is object permanence, which is the ability to know that objects continuously exist through space and time, even when they are hidden [3]. In humans, object permanence develops through six main stages: in the first three stages (i.e., stage 1: development of reflexes, stage 2: development of habits, stage 3: development of coordination between vision and prehension), infants show no object permanence. [3]. Before approaching the first year of age, however, they understand objects as separate entities existing even when they are not visible (stage 4) and can locate objects after visible (stage 5) and invisible displacements (stage 6) [3–6]. Object permanence is also widespread in species other than humans [7], for example, it has been shown in primates [8–16], birds [17–24], dogs (Canis familiaris; [25–27]), cats (Felis catus; [27, 28]), goats (Capra aegagrus hircus; [29–31]), sheep (Ovis orientalis aries; [31, 32]), giraffes (Giraffa carmelopardalis; [33]) and dolphins (Tursiops truncatus; [34]), just to name a few.
Another crucial cognitive skill is the ability to recall the position of objects or other animals after different delays of time. Short-term memory, for instance, is very common in different taxa [7], and has been reported in primates [8, 12, 35], birds [36–38], dogs [25, 39], cats [25, 27, 39], goats [29], sheep [40], giraffes [33] and horses (Equus caballus; [41]) among others. Studies in ungulates, a less studied taxon in this regard, have shown that giraffes can successfully recall the position of hidden food after delays of up to 30 seconds [33], whereas horses can store information about hidden food for at least 20 seconds [41].
Causal understanding, defined as the understanding that one event is the consequence of another, might also be important to deal with socio-ecological challenges [42]. Causal understanding, for instance, might facilitate the retrieval of embedded food (e.g. trap tube task: [43, 44]; e.g., tool-use in crows: [45]) and allow individuals to better predict where and when food will be available [46]. From 3 years of age, human children are able to solve causality tasks in which they are presented with two opaque containers, only one being baited, and they receive either acoustic or visual cues about the location of the reward, by for instance shaking either the baited or the non-baited container [47]. Species other than humans can also use acoustic cues to infer the location of food, including primates [48], corvids (Garrulus glandarious; [49]), pigs (Sus scrofa domestica), and wild boars (Sus scrofa scrofa; [50]). Pigs and wild boars, for instance, were able to locate food in one out of two containers, if the baited one provided an acoustic cue when being shaken. However, when the empty container was shaken, they failed to infer that the food was in the other container [50]. When using visual cues (i.e., lifting the baited or the non-baited container), also goats and sheep showed an understanding of causal relationships [31].
The ability to understand object properties is also crucial for several species. In humans, infants from 5 months of age understand object properties like solidity, and at 9 months they preferentially search for objects where a protuberance marks a hidden object under a cloth lying flat on a table, suggesting that these skills may be part of our innate core knowledge [5,6,51–57,but see 58]. Moreover, when seeing one object disappear behind one out of two occluders of different size and/or shape, children from 3.5 months of age preferentially search for the object behind the occluder having the proper size and/or shape to hide the object [57]. These skills might be very useful also for species other than humans. By understanding which objects can visually occlude others, for instance, animals might make predictions about where predators might be hiding [22, 59, 60]. Newborn domestic chicks (Gallus gallus), indeed, can successfully locate an object behind the only occluder compatible with the object’s shape, and they do it without any previous experience with objects, suggesting that these skills might be part of their innate core knowledge [22]. However, experience might also be important to acquire a better understanding of object properties, as has been shown in horses [61] and pigs [50].
Finally, animals can also rely on other object properties, like gravity, to effectively solve socio-ecological challenges. Humans, for instance, show the first evidence of gravity understanding from 7 months of age, looking longer at a test event with inappropriate acceleration where a ball moved up-/downward while speeding up/slowing down [62–65]. However, also other species can use gravity as a cue to locate food in different experimental contexts. Several species, for instance, can successfully locate falling objects, including great apes (Gorilla gorilla, Pongo pygmaeus, Pan troglodytes, Pan paniscus; [66]), cotton-top tamarins (Saguinus oedipus oedipus; [67]), and dogs [68]. However, when the trajectory of the falling object gets redirected (e.g. by letting objects fall through crossed tubes), children show a gravity bias until around 3 years of age, failing to account for the presence of the tubes and still searching below the releasing point [66, 69]. This gravity bias is present in several other species, including cotton-top tamarins [70], macaques (Macaca mulatta, Macaca arctoides, [71]), and dogs [68], whereas great apes can successfully locate food falling through crossed tubes [66].
Although these cognitive skills (i.e. object permanence, short-term memory, causality, understanding of object properties, and understanding of gravity) are likely crucial to face a variety of socio-ecological challenges, it is currently unclear how these skills are distributed across species, and which factors best predict this distribution. Some of these skills, for instance, object permanence and understanding of object properties, might be part of the innate core knowledge of several taxa [22], although experience might also be important to acquire a better understanding of object properties [50, 61]. Other skills, however, might have emerged in different species as a response to the specific socio-ecological challenges faced during evolution and might be largely independent of the living conditions experienced by single individuals. Researchers have proposed different evolutionary hypotheses on the distribution of cognitive skills, which are not mutually exclusive. Here, we will focus on the three hypotheses that have been widely explored in other studies.
First, some authors have proposed that species with larger dietary breadth (i.e. consuming a higher number of dietary categories) may more likely exploit novel food sources and might have thus evolved enhanced cognitive skills to better cope with this variation [72]. In primates, there is indeed evidence that larger dietary breadth is linked to enhanced cognitive skills such as inhibition, but it is still unclear whether dietary breadth also has the same explanatory power in other taxa [73]. Second, species with high levels of fission-fusion dynamics (i.e. experiencing frequent changes in subgroup size and composition; high level meaning highly fluid with either relatively stable or flexible subgroup membership; 74) might show an increase in some cognitive skills, like memory to remember the identity and social relationships of other group members that are often in other subgroups, and inferential skills to effectively deal with fragmentary information about absent group members [74, 75]. Third, domesticated species have been selected for skills and traits that facilitate their interaction with humans and are usually considered to be more playful and explorative than their wild counterparts [76, 77]. Therefore, domesticated species may be more interested in anthropogenic objects and more likely to explore them, and thus might have a higher chance to acquire important information on their properties during their lives [29, 50, 78].
In this study, we aimed to assess how different cognitive skills are distributed across captive individuals belonging to different ungulate species. We selected ungulates as a study model for two main reasons. Firstly, despite being economically crucial for humans, ungulates are a still largely under-studied taxon [30, 79, 80]. Secondly, ungulate species show an impressive variety of socio-ecological characteristics [81] and thus constitute an ideal model to contrast different evolutionary hypotheses on the emergence of cognitive skills. In this study, we compared the performance of dwarf goats (Capra aegagrus hircus), llamas (Lama glama), guanacos (Lama guanicoe), Grevy´s zebras (Equus grevyi) and rhinos (Diceros bicornis michaeli) in a series of tasks testing their object permanence, short-term memory, causality, understanding of object properties and understanding of gravity. We used the same controlled experimental procedures for all study subjects to allow more accurate comparisons [8, 31, 66, 82].
Based on existing literature (e.g., [83–90]), we predicted that all species would show object permanence (Prediction 1), as this is part of their core knowledge, but that there would be inter-specific variation in the other tasks. In particular, if dietary breadth explained the distribution of cognitive skills across taxa, we would predict that species consuming a higher number of dietary categories (i.e., goats) would perform better than the others (i.e., llamas, guanacos, Grevy´s zebras and rhinos) in the other tasks (Prediction 2a). If fission-fusion levels explained the distribution of cognitive skills, we would instead predict that species with higher levels of fission-fusion dynamics (i.e., goats, Grevyi’s zebras) would perform better than species with lower levels of fission-fusion dynamics (i.e., llamas, guanacos, rhinos), especially in tasks requiring memory and inferential skills (i.e., the short-term-memory and the causality tasks, see below; Prediction 2b). If domestication explained the distribution of cognitive skills across taxa, we would predict that domesticated species (i.e., goats, llamas) would perform better than non-domesticated species (i.e., guanacos, Grevy’s zebras, rhinos; Prediction 2c).