Social learning of feeding behaviour in pigs: Effects of neophobia and familiarity with the demonstrator conspecific
Introduction
Food preferences and aversions are strongly influenced by individual learning experience (Dwyer et al., 2009, Sclafani, 2004, Sclafani and Zukerman, 2009) but also are determined by social interactions (Galef and Whiskin, 1997, Galef and Whiskin, 2001). In natural environments, social learning increases the probability of survival, especially in young individuals that benefit from learning behaviours from experienced animals (Galef and Giraldeau, 2001, Thornton and Malapert, 2009). It has been reported in several species that food information can be transferred from one individual to another through social learning (Oostindjer et al., 2011, swine; Posadas-Andrews and Roper, 1983, rats; Provenza and Balph, 1987, ruminants). In rats, when a conspecific (demonstrator) ate a new flavoured food, another rat (observer) learnt to prefer that food in a future exposure after a brief interaction with this experienced animal because of the contact with food odours in the breath of the demonstrator rat. This learning is not affected by the age or familiarity of the demonstrator and even appeared when such an act led to inferior benefits (Galef, 1996, Galef and Whiskin, 2008a). However, a common observation in the social learning literature is that individuals often copy kin with the expectation of obtaining the same rewards (Coussi-Korbel and Fragaszy, 1995, Laland, 2004). Evolutionary theory indicates that familiar animals also share a common environment and probably they are genetically related (Laland, 2004, Valsecchi et al., 1996), which make social learning an adaptive behaviour (Laland, 2004).
Pigs are highly social animals and begin to form social relationships with littermates within hours of birth (Graves, 1984). Nevertheless, there have been only a few studies of social learning of feeding behaviour in pigs. Nicol and Pope (1994) and Held et al. (2000) showed that an inexperienced pig could follow an experienced pig and learn about the location of food, and Morgan et al. (2001) also demonstrated that feed intake is enhanced when an inexperienced pig is housed with an experienced conspecific. However, a “follow the leader” can be a local enhancement phenomenon in which the observer animal is attracted to the place that demonstrator visits.
At weaning, piglets face three main challenges in the intensive pig-farming industry, including changes in the physical environment, the psychological stress that accompanies moving and mixing animals, and a major change in feed composition. Early weaned piglets have to find their own feed, which it is more bulky and dry (usually >88% of dry matter), less digestible than milk, and composed of ingredients that piglets have not previously encountered. In these conditions most weaned piglets are reluctant to eat the new feed, leading to anorexia on the first days after weaning (Fraser, 1984, Moeser et al., 2012, Pluske et al., 2007). Neophobic avoidance of new feeds may seem a maladaptive process for omnivorous species that need to consume a varied diet to obtain adequate nutrition and may become critical in intensive production systems where new diets have to be incorporated during a short period of time (Provenza and Balph, 1988). However, neophobia may be reduced through a learning process before or after birth involving contact with flavour cues and associations between those components and positive consequences (Ackroff and Sclafani, 2010, Hepper and Wells, 2006, Mennella et al., 2001, Oostindjer et al., 2009, Oostindjer et al., 2010).
Social interactions with experienced pigs could help naïve pigs to learn about environment conditions with minimal trial and error. Through social learning, individuals do not need to search their entire home range, or sample potentially toxic foods (Laland, 2004). The aim of this study, composed of three experiments, was to investigate if social learning in pigs could help to establish preferences towards a particular ingredient or flavour after interacting with a conspecific that has eaten these compounds. In the first experiment we hypothesized that pigs can learn to prefer a flavoured feed following brief interactions with conspecifics during the post-weaning period, without participating or watching during the demonstrator feed intake. We also hypothesized that this learning could be affected by the familiarity of the demonstrator. In a second experiment, we established whether these preferences were affected by the type of familiarity (penmates vs. littermates) and finally in the third experiment we studied if social learning could increase preferences for a diet over the previously known unflavoured feed.
Experiments were conducted at the weanling unit of the pig facilities belonging to the Universitat Autònoma de Barcelona (UAB). Experimental procedures were approved by Ethical Committee on Animal Experimentation of the UAB. (CEAAH 1406).
Section snippets
Subjects
A total of 448 entire male (224) and female (224) pigs ([Large White × Landrace] × Pietrain) of 49d of age (3 weeks after weaning) were used (256 in Experiment 1, 64 in Experiment 2 and 128 in Experiment 3). Animals were individually identified at birth by using a plastic ear tag and they stayed with their mother and littermates inside the farrowing crates (standard farrowing create, 0.5 m wide, 2.0 m long and 1.03 m high) and their corresponding area for piglets (total available area 4.63 m2; 4.15 m2
Statistical analysis
Pen feed consumption during the observers choice test was analyzed with ANOVA by using mixed linear models with the MIXED procedure of the statistical package SAS® (SAS Inst. Inc., Cary, NC), taking into account the effects of the group (familiar vs. unfamiliar in experiment 1; littermate vs. penmate in experiment 2; Pre-exposed vs. control in experiment 3), flavours eaten by demonstrators (aniseed or garlic), sex (experiment 1), feed consumed (DEM-feed or OTH-feed) and the interaction between
Familiar vs. unfamiliar demonstrators (experiment 1)
The average flavoured feed (aniseed or garlic) intake by the demonstrator pens (4 pigs/pen) after 30 min of exposure before social contact was 324 g/pen; SEM 34.5 g (81 g/pig). The intake of flavoured feeds by the observer's pens during the choice test is summarized in Fig. 1. The feed offered previously to demonstrator pigs had an effect on feed preferences of familiar observers (penmates) but not unfamiliar observers (next door pen observers) (GROUP × FEED CONSUMED; F 1,28 = 11.68, P = 0.002).
Discussion
The present experiments shows that pigs, like rats (Galef, 1995) and non-human primates (Hopper et al., 2011), were able to learn a preference for flavoured feeds following social interactions with a conspecific. A brief contact with a demonstrator that recently ate a flavoured diet was enough to change the feeding behaviour of naïve observers. This could have a great importance in some critical stages of pig development, reducing the possible energy costs associated with individual trial-and
Acknowledgements
The present study was supported by the Spanish Government (MCI, project PET2008_0002). We also want to thank the Chilean Government research fellowships “Becas Chile”, and Alexandra Solà for the collaboration during experiments.
References (45)
- et al.
Flavor preferences conditioned by post-oral infusion of monosodium glutamate in rats
Appetite
(2010) - et al.
On the relation between social dynamics and social learning
Anim. Behav.
(1995) - et al.
Individual recognition and the dominance hierarchy in the domesticated pig. The role of sight
Anim. Behav.
(1974) The role of behavior in swine production: a review of research
Appl. Anim. Ethol.
(1984)The adaptive value of social learning: a reply to Laland
Anim. Behav.
(1996)- et al.
Social influences on foraging in vertebrates: causal mechanisms and adaptive functions
Anim. Behav.
(2001) - et al.
Social exploitation of intermittently available foods and the social reinstatement of food preference
Anim. Behav.
(2000) - et al.
Interaction of social and individual learning in food preferences of Norway rats
Anim. Behav.
(2001) - et al.
Effects of environmental stability and demonstrator age on social learning of food preferences by young Norway rats
Anim. Behav.
(2004) - et al.
‘Conformity’ in Norway rats?
Anim. Behav.
(2008)