The effect of domestication and ontogeny in swine cognition (Sus scrofa scrofa and S. s. domestica)

Abstract

Domesticated animals show physical, behavioural and cognitive differences from their closest wild relatives. This may have resulted from the former's long and continued selection by humans throughout history, but in some cases it could just reflect developmental differences between wild and domestic animals, given that their environments usually differ significantly. In order to investigate possible effects of domestication and ontogeny on swine cognition, we tested wild boars and two groups of domestic pigs living in more and less enriched conditions. In an object choice paradigm subjects had to find food hidden in one of two containers. They received either a physical cue (i.e., the slope of the board hiding the food, the presence or absence of noise from a shaken container, the sight of a baited container changing position) or a human social cue (i.e., touching, pointing, gazing). According to the domestication hypothesis, given similar rearing conditions domestic pigs should perform better than wild boars when receiving social cues but worse when receiving physical cues. According to the developmental hypothesis, more experienced swine should perform better than less experienced swine both in the physical and in the social domain. Subjects performed better when provided with cues on which they had received adequate experience from their environment, thus providing support to the developmental hypothesis. We conclude by suggesting that specific experience on particular stimuli rather than general experience on a wider range of stimuli may explain swine ability to solve both social and physical tasks.

Introduction

Domestication has been defined as a process of natural and artificial selection, with adaptation to an often captive environment achieved through genetic changes occurred over generations and environmentally induced developmental changes recurring during each generation (Price, 1984). In comparison to their closest wild relatives, domestic animals show greater gregariousness, less wariness, more playfulness, earlier sexual maturity and more frequent receptivity (Zeder, 2006). Some of these behavioural traits may have been actively (although not necessarily intentionally) selected by humans to increase benefits or to facilitate management, whereas others may be by-products of this selection or mere consequences of life in captivity.

Compared to natural environments, captive environments are usually more stable and predictable. The space available and the number of conspecifics are limited, the likelihood of being attacked by a (non-human) predator is low, resources usually appear recurrently at the same time and location and they are easily accessible. Moreover, domestic animals live close to and depend on humans for obtaining food. It is possible that their long history of domestication has impoverished their ability to cope with the physical environment, with human intervention relaxing selective pressures on species’ specific behavioural patterns (Frank, 1982). On the other hand, this background may have equipped them with the ability to use human cues for their own benefit (Hare et al., 2002, Hare and Tomasello, 2005, Miklosi et al., 2003, Virányi et al., 2008).

The main aim of the current study was to compare the cognitive skills of domestic and wild animals, both in the physical and in the human social domains, using swine as a model. Indeed, wild boars (Sus scrofa scrofa) and domestic pigs (Sus scrofa domestica) are reported to share common wild ancestors (Larson et al., 2005, Larson et al., 2007). Swine are especially interesting because, unlike the other main domesticates (i.e., goat, sheep, cattle and dog), they are omnivorous. For that reason, wild boars require good general skills to exploit their complex natural physical environment, whereas domestic pigs might have lost some of these skills in their captive environment, as they are potentially redundant (but see Held et al., 2002b). On the other hand, being omnivorous has determined a particular domestication history for pigs, characterized by a close contact with humans, that partially resembles that of dogs. In an initial phase, wild boars (especially the ones that were less scared of humans) might have been attracted to leftover food and cultivated plants in human settlements. Deemed useful as meat stock and in order to recycle waste, some of them (especially the tamer ones) were probably tolerated in the camps or, alternatively, caught and kept in captivity (Hongo and Meadow, 1998). Such close contact with humans might have enhanced those abilities related to the use of human cues by domestic pigs, although probably to a lesser extent than dogs which, in addition to being camp scavengers and potential meat stock, served as hunting companions and house pets (Clutton-Brock, 1995, Hongo and Meadow, 1998).

However, when comparing domestic animals and their wild relatives one needs to consider that they usually experience different environments throughout their ontogeny and cognitive differences could therefore be explained by developmental factors rather than evolutionary ones. A second aim of the present study was consequently to assess the extent to which possible cognitive differences between wild boars and domestic pigs reflect genetic variation or simply porcine behavioural flexibility during ontogeny.

To investigate the potential effects of domestication and ontogeny on swine cognition we used an object choice paradigm in which subjects have to choose between two opaque containers, only one of which has been baited with a food reward. The experimenter provides a physical or a social cue as to where the food has been hidden. Physical cues are given when the subject is provided with physical information about food location, for example the inclination of a board that has food below it, the noise coming from a shaken container that has food inside it or the visible displacement of a baited container from one location to another. The choice of the correct container implies that the subject understands something about basic principles of the physical world, such as the causal connection between objects, how objects affect the orientation of other objects and produce noises under different circumstances or the way objects move (Bräuer et al., 2006, Call, 2004, Call, 2006, Call, 2007). Social cues, on the other hand, are given when the behaviour of the experimenter provides information about where the food reward is hidden. This information can be either behavioural (i.e., reaching towards the correct container) or communicative (i.e., if the experimenter is looking at the subject while indicating the food location using gestures such as pointing, gazing or touching the correct container). To what extent animals use these gestures and understand their communicative intent or whether simpler mechanisms like local enhancement are at play is still a matter of lively debate (Miklosi and Soproni, 2006, Povinelli et al., 1997).

Previous studies have investigated domesticated species’ abilities to use social cues in order to locate hidden food. For example, domesticated species reliably use touching (horses: McKinley and Sambrook, 2000; goats: Kaminski et al., 2005) or pointing as a cue (cats: Miklosi et al., 2005; horses: Maros et al., 2008, Proops et al., 2010; goats: Kaminski et al., 2005). Moreover, domestic dogs show a flexible use of a variety of social cues from the first trial onwards and even at the age of 6 weeks, they appear to perceive the situation as being communicative and they are more adept at using human cues than their wild relatives, the wolves (e.g., Bräuer et al., 2006, Hare et al., 1998, Hare et al., 2002, Hare et al., 2010, Miklosi and Soproni, 2006, Riedel et al., 2008). Some authors have therefore argued that, at least in dogs, the ability to read human cues has been mainly developed during domestication, with ontogeny playing a less important role. However, other studies suggest that ontogenetic experience is important to understand human social cues, with dogs’ ability to use human cues improving with age, and wolves raised with intensive social contact to humans also being able to read complex human social cues (e.g., Barrera et al., 2011, Dorey et al., 2010, Elgier et al., 2009, Udell et al., 2008, Udell et al., 2010a, Udell et al., 2010b).

On the other hand, very few studies have investigated domesticated species’ abilities to use physical cues to locate hidden food. These studies have shown that, in contrast to their good performance in social tasks, both cats and dogs can only master the easiest conditions of transposition tasks (i.e., object permanence tasks; cats: Doré et al., 1996; dogs: Collier-Baker et al., 2004, Rooijakkers et al., 2009). When Bräuer et al. (2006) compared the performance of chimpanzees and domestic dogs on a series of object choice tasks, dogs were especially skillful when being provided with a social cue and chimpanzees performed better when provided with physical cues. The authors argued that domestic dogs might have evolved human cue reading skills during the domestication process, but might have lost some of their skills for understanding physical cues, since humans solve many causal problems for them (Bräuer et al., 2006, Frank, 1980).

Previous studies on domestic pigs have shown that they have good spatial memory (Laughlin et al., 1999, Mendl et al., 1997) and can discriminate food sites on the basis of quantity (Held et al., 2005). Pigs are also able to use cues provided by conspecifics to find food, following informed partners to a food location, and they adjust their foraging behaviour to maximize food intake when they are victims of exploitation (Held et al., 2000, Held et al., 2002a). However, to our knowledge swine have not been tested in object choice tasks before, and no direct experimental comparison between wild boars and domestic pigs has so far been conducted.

In the present study we aimed at doing a first exploration of the roles that domestication and ontogeny might play on swine cognition. With this purpose, we systematically compared wild boars and domestic pigs using a series of object choice tasks which have already been successfully used with several other species to measure their ability to use social and physical cues to infer the location of hidden food (see Bräuer et al., 2006). We compared (i) the performance of wild boars and domestic pigs living in similar environments (WB+ and DP+, respectively) and (ii) the performance of domestic pigs living in environments that allowed them more versus less physical and social experience (DP+ and DP−). We wanted to contrast two different hypotheses, (i) whether domestic pigs are more capable than wild boars at using human social cues to locate hidden food, but less adept at using physical cues (domestication hypothesis, or DOM), and (ii) whether swine whose rearing conditions have allowed more physical and social experience during ontogeny perform better than swine who have been raised in “poorer” rearing conditions (developmental hypothesis, or DEV_GENERAL). An alternative version of the DEV hypothesis would be that (iii) rather than generally richer conditions (i.e., exposure to a greater variety of stimuli) leading to a generally better performance, it is specific experience (with specific stimuli) which allows the mastery of related specific problems, regardless of them belonging to the physical or the social domain (DEV_SPECIFIC).