Environmental enrichment induces optimistic cognitive biases in pigs
Introduction
The development of objective methods for assessing the affective (or emotional) states of non-human animals is a crucial step in improving animal welfare (e.g. Dawkins, 2008). In human psychology, there is an extensive body of literature showing that affective state can influence cognitive processes (Bar-Haim et al., 2007, Eysenck et al., 1991, Williams et al., 1997). Typically, negative affective states are accompanied by greater attention to threatening stimuli and an increased likelihood that ambiguous information will be interpreted pessimistically, whereas more postive states are accompanied by more optimistic judgements. The term ‘cognitive bias’ is used as a general label for these effects of affective state on cognitive processes (Mendl et al., 2009). The existence of affectively induced cognitive biases in humans has lead to the suggestion that measures of cognitive bias might provide a novel method for objectively assessing both positive and negative affective states in non-human animals (Mendl et al., 2009, Paul et al., 2005). In animal studies, ‘optimism’ and ‘pessimsim’ are defined operationally as respectively, an increased expectation of reward in the face of ambigous information and an increased expectation of punishment in the face of ambiguous information. No assumption is made about whether these objective biases in decision-making are accompanied by subjective emotional states. The cognitive bias approach has a number of attractive features compared with exisiting methods for welfare assessment, including: clear a priori predictions about the types of biases expected, greater selectivity for the valence of an emotional state as opposed to the level of arousal involved, the ability to assess postive as well as negative emotional states, and finally, the non-invasive nature of the techniques involved (Mendl et al., 2009, Paul et al., 2005). In support of the hypothesis that cognitive bias could be a useful welfare assessment tool, there is evidence from a range of species including rats (Brydges et al., 2011, Burman et al., 2008a, Enkel et al., 2010, Harding et al., 2004), European starlings (Bateson and Matheson, 2007, Brilot et al., 2010, Matheson et al., 2008), sheep (Doyle et al., 2010a, Doyle et al., 2010b, Doyle et al., 2011), dogs (Mendl et al., 2010a) domestic chicks (Salmeto et al., 2011) and even honeybees (Bateson et al., 2011) that animals hypothesised to be in more negative affective states are typically more pessimistic, whereas animals hypothesised to be in more postive states are more optimistic.
There is mounting evidence that animals housed in enriched conditions have better welfare, and hence by assumption more positive affective states, compared to those housed in more barren environments (e.g. Balcombe, 2006). This belief is supported by the cognitive bias assessments, that report more optimistic cognitive biases in both laboratory rats and European starlings currently housed in more enriched or more stable cages (Bateson and Matheson, 2007, Brydges et al., 2011, Harding et al., 2004, Matheson et al., 2008). There is also a suggestion that the recent history of an animal can be important in determining its affective state. For example, Bateson and Matheson (2007) found that starlings only exhibited a pessimistic cognitive bias in barren cages when they had recently been moved from enriched cages. Together these studies suggest that cognitive bias could be a useful tool for measuring the impact of an animal's environment on its affective state and hence its welfare.
In the current study we focus on assessing the impact of different housing practices on pig welfare. A range of different housing and rearing practices are used for pigs, some of which involve substantial changes in environment, for example outdoor reared pigs being finished inside. There are 5 million pigs on UK farms (DEFRA, 2010), so numerically, pig welfare is important. The recent European Commission funded Welfare Quality research project's “Assessment Protocols for pigs” (2009), as well as those for cattle and poultry, emphasise the importance attributed to assessing positive emotional states in welfare assessment of our food producing animals. Currently such affective states are captured by Qualitative Behaviour Assessment terms (e.g. depressed, happy, content, frustrated, active, relaxed), (e.g. Wemelsfelder, 2007) which are scored subjectively by an independent auditor and the results entered into a weighted formula to produce a score (Welfare Quality, 2009). Tests of cognitive bias would offer a complementary, objective measure to support these subjective assessments.
The aim of our study was to investigate whether a cognitive bias methodology could be used to assess the effects of environmental enrichment on affective state in pigs. Provision of various types of environmental enrichment has been found to improve traditional welfare indicators (e.g. health and production parameters, tail biting, aggression, fear of humans, exploratory behaviour and play) in a number of other studies with pigs (for reviews see: Bracke et al., 2006, van de Weerd and Day, 2009) and our hypothesis was therefore that pigs currently housed in enriched pens would display more optimistic cognitive biases than pigs currently housed in barren pens. We also sought to investigate the extent to which the affective state of pigs is influenced by their previous environmental experiences. Based on a number of studies showing that animals, including pigs, are particularly sensitive to a decrement in environmental quality (e.g. Bateson and Matheson, 2007, Burman et al., 2008b, Melotti et al., 2011, Oostindjer et al., 2011a, Oostindjer et al., 2011b), we hypothesised that we would see greater pessimism in pigs currently housed in a barren environment if they had previously experienced an enriched environment. We assessed the cognitive bias of individual pigs using a go/no-go judgement bias task based on a learnt discrimination of two auditory cues one of which predicted a positive and one a negative outcome (i.e. similar to the the task used by Harding et al., 2004). We defined optimism operationally as a higher proportion of responses to an amibiguous cue as if it were the cue predicting the positive outcome, and pessimism as a higher proportion of responses to an ambiguous cue as if it were the cue predicting the negative outcome.
Section snippets
Animals and housing environment
Two groups, each of five Large White × Landrace gilts, approximately 12 weeks of age and weighing 35 kg at entry to the experiment, were assigned randomly to be housed in either an enriched or barren environment. The barren environment (in accordance with the minimum legal provision for pigs housed intensively under EC Directive 2008/120/EC) provided 1.2 m2 of space per pig, had partially slatted concrete flooring and enrichment was provided only in the form of a wood log on the floor. The enriched
Task acquisition
It took 9 days training (i.e. 180 trials) for all the pigs to reach criterion in approach to the hatch for reward following the positive cue. It took a further 10 days of training (i.e. 200 trials) for all the pigs to reach criterion on the go/no-go discrimination task. Thus, all 10 pigs acquired a signficant discrimination of the positive and negative cues. In the final 3 days of discrimination training there was no significant difference in the proportion of correct responses between Group EBE
Discussion
Pigs currently housed in an enriched enviorment were more likely to respond to an ambiguous auditory cue by approaching a hatch at which food had previously been received than pigs currently housed in a barren environment. This optimistic cognitive bias was also evident in the pigs’ latency to approach the hatch, with pigs currently housed in the enriched environment responding more quickly to the amibiguous cue than when housed in the barren environment. Analyses of the approach data also
Conclusion
This study is the first to successfully apply a cognitive bias methodology to pigs and the first to demonstrate a change in cognitive bias consequent on environmental enrichment in farm livestock. We found that environmental enrichment induces optimistic cognitive bias indicative of a postive affective state. Validating this methodology for use in a farm species is an important contribution to studies of animal welfare, giving a novel and objective insight into an animal's affective state. This
Acknowledgements
The authors would like to thank UFAW for funding this project. They would also like to thank Liz Paul, Mike Mendl, Dan Weary, Richard Parker and Kenny Rutherford for sharing their experiences of cognitive bias protocols.
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