Complex, context-dependent decision strategies of archerfish, Toxotes chatareus

Operant conditioning is fundamental to many animal behaviour experiments, including the alternative forced-choice (AFC) task, a powerful and popular paradigm for establishing learning and discrimination abilities across a wide array of species. One frequently overlooked aspect of this paradigm is the relative importance of the positive (S+ or ‘target’) and negative stimulus (S− or ‘distractor’). It is often assumed that subjects learn to associate S+ with a reward. However, it is equally possible that they learn to associate S− with the absence of a reward. The rule learned may have repercussions for the design of experiments, and may also provide information about the decision strategies employed by a particular animal or species. Archerfish are becoming increasingly popular as a model for testing cognition in lower vertebrates. We conducted three experiments to explore how archerfish learn to complete a common type of forced-choice test. In the first experiment, we showed that archerfish were able to discriminate a range of shapes in an AFC task. In the second experiment, we found that replacing S− with novel stimuli caused a greater disruption in performance than replacing S+. In the final experiment we showed that archerfish: (1) were probably using complex decision rules; (2) made context-dependent choices; and (3) examined some or all of the stimuli before making a decision when faced with multiple stimuli. Our results show that archerfish have a flexible learning strategy which may facilitate exploitation of novel food sources. The discovery that archerfish avoid negative stimuli fits with their generalist feeding ecology in which they may learn to avoid distasteful/toxic prey. At the same time the fish demonstrate a willingness to try new prey, which have the potential to offer a greater reward than familiar target prey.