zoo:logic

New research has shown that Atlantic salmon (Salmo salar) experience a feeling akin to frustration when they are not given a reward they are expecting to receive - a response previously only observed in mammals and birds. Debates over the ethics of fishing often throw up questions of whether fish are ‘conscious’ and have an awareness of pain, which has fuelled a fair amount of research in the area. Fish have been shown to be capable of responding to classical conditioning and to have long-term memories; however, we are still unsure to what extent their cognitive abilities are linked to conscious moods and emotions. This concept was studied in the salmon using a model commonly used in mammalian research called omission of expected reward (OER). In these experiments, animals are conditioned to associate a certain stimulus with a positive reward, such as food, and are then subjected to the stimulus without receiving the reward to record how they react. In mammals, OER has consistently been shown to cause animals to become stressed and aggressive.

Six groups, each consisting of 200 fish, were conditioned to associate a flashing light with feeding over a period of 22 days. By the end of this period, the fish showed attraction to the light due to association with the food reward, as opposed to their initial reaction of avoiding it. Three of the groups were then subjected to OER for 9 days - the fish were fed three times a day, and at two of these mealtimes, the expected food reward was delayed by 30 minutes. The other three groups carried on as normal, acting as controls.

When the groups were compared, OER groups showed higher aggression and greater hierarchy, causing some individuals to grow more quickly at the expense of others - interestingly, even during the one meal a day when the reward was provided immediately, aggression levels remained high. Stress levels were measured by detecting the concentration of cortisol (a hormone which is involved in stress response) in the blood, but unlike the variation seen in aggressive behaviour, these were the same across all groups, suggesting that although there were behavioural signs of stress this did not translate to a physiological stress reaction.

There are two possible explanations for the variation in aggressive behaviour:
- Dominant individuals may be trying to keep their position for prime access to food in expectation of the coming reward
- Aggression triggered by the stressful situation may be being displaced towards other individuals to help in coping with the conditions.
In either case this leads to stronger hierarchy and more uneven distribution of resources, as was observed in this study. 

The overall conclusion is that fish respond behaviourally to frustrating conditions just like birds and mammals, suggesting this could be an adaptive response to unpredictable environments that has been conserved throughout vertebrate evolution. While we cannot yet conclude that fish definitely experience conscious emotional states, the results do highlight the importance of regular routine for domestic or farmed fish in order to reduce aggressive interactions between individuals that may be detrimental to the health of the population.

Ref: Vinas M. A. et al., 2012. Omission of expected reward agitates Atlantic salmon (Salmo salar). Animal Cognition  Online first [link]