Environmental enrichment improves cognitive flexibility in rainbow trout in a visual discrimination task: first insights.

Research on fish cognition provides strong evidence that fish are endowed with high level cognitive skills. However, most studies on cognitive flexibility and generalization abilities, two key adaptive traits for captive animals, focused on model species, and farmed fish received too little attention. Environmental enrichment was shown to improve learning abilities in various fish species, but its influence on cognitive flexibility and generalization abilities is still unknown. We studied farmed rainbow trout (Oncorhynchus mykiss) as an aquaculture model to study how environmental enrichment impacts their cognitive abilities. Using an operant conditioning device, allowing the expression of a motivated choice, we measured fish cognitive flexibility with serial reversal learning tests, after a successful acquisition phase based on two colors discrimination (2-alternative forced choice, 2-AFC), and their ability to generalize a rewarded color to any shape. Eight fish were divided into two groups: Condition E (fish reared from fry stages under enriched conditions with plants, rocks and pipes for ~9 months); Condition B (standard barren conditions). Only one fish (condition E) failed in the habituation phase of the device and one fish (condition B) failed in the 2-AFC task. We showed that after a successful acquisition phase in which the fish correctly discriminated two colors, they all succeeded in four reversal learnings, supporting evidence for cognitive flexibility in rainbow trout. They were all successful in the generalization task. Interestingly, fish reared in an enriched environment performed better in the acquisition phase and in the reversal learning (as evidenced by fewer trials needed to reach the learning criterion), but not in the generalization task. We assume that color-based generalization may be a simpler cognitive process than discriminative learning and cognitive flexibility, and does not seem to be influenced by environmental conditions. Given the small number of individuals tested, our results may be considered as first insights into cognitive flexibility in farmed fish using an operant conditioning device, but they pave the way for future studies. We conclude that farming conditions should take into account the cognitive abilities of fish, in particular their cognitive flexibility, by allowing them to live in an enriched environment.

Positive effects of bubbles as a feeding predictor on behaviour of farmed rainbow trout.

Occupational enrichment emerges as a promising strategy for improving the welfare of farmed animals. This form of enrichment aims to stimulate cognitive abilities of animals by providing them with more opportunities to interact with and control their environment. Predictability of salient daily events, and in particular predictability of feeding, is currently one of the most studied occupational enrichment strategies and can take several forms. In fish, while temporal predictability of feeding has been widely investigated, signalled predictability (based on a signal, such as light or sound) has received little attention. Depending on the type of predictability used and the ecology of the species, the effects on fish welfare often differ. The present study aimed to determine which feeding predictability would be most appropriate for rainbow trout, the main continental farmed fish in Europe, and what the consequences might be for their welfare. We tested four feeding predictability conditions: temporal (based on time of day), signalled (based on bubble diffusion), temporal + signalled (based on time and bubble diffusion), and unpredictable (random feeding times). Behavioural and zootechnical outcomes recorded were swimming activity, aggressive behaviours, burst of accelerations, and jumps, emotional reactivity, and growth. Our results showed that rainbow trout can predict daily feedings relying on time and/or bubbles as predictors as early as two weeks of conditioning, as evidenced by their increased swimming activity before feeding or during feed omission tests, which allowed to reinforce their conditioned response. Temporal predictability alone resulted in an increase in pre-feeding aggressive behaviours, burst of accelerations, and jumps, suggesting that the use of time as the sole predictor of feedings in husbandry practices may be detrimental to fish welfare. Signalled predictability with bubbles alone resulted in fewer pre-feeding agonistic behaviours, burst of accelerations, and jumps than in the temporal predictability condition. The combination of temporal and signalled predictability elicited the highest conditioned response and the level of pre-feeding aggression behaviours, burst of accelerations and jumps tended to be lower than for temporal predictability alone. Interestingly, fish swimming activity during bubble diffusion also revealed that bubbles were highly attractive regardless of the condition. Rainbow trout growth and emotional reactivity were not affected by the predictability condition. We conclude, therefore, that the use of bubbles as a feeding predictor could represent an interesting approach to improve rainbow trout welfare in farms, by acting as both an occupational and physical enrichment.

Rainbow trout discriminate 2-D photographs of conspecifics from distracting stimuli using an innovative operant conditioning device.

Cognitive abilities were studied in rainbow trout, the first continental fish production in Europe. Increasing public concern for the welfare of farmed-fish species highlighted the need for better knowledge of the cognitive status of fish. We trained and tested 15 rainbow trout with an operant conditioning device composed of self-feeders positioned in front of visual stimuli displayed on a screen. The device was coupled with a two-alternative forced-choice (2-AFC) paradigm to test whether rainbow trout can discriminate 2-D photographs of conspecifics (S+) from different visual stimuli (S-). The S- were applied in four stages, the last three stages representing increasing discrimination difficulty: (1) blue shapes; (2) black shape (star); (3) photograph of an object (among a pool of 60); (4) photograph of another fish species (among a pool of 60). Nine fish (out of 15) correctly managed to activate the conditioning device after 30-150 trials. The rainbow trout were able to discriminate images of conspecifics from an abstract shape (five individuals out of five) or objects (four out of five) but not from other fish species. Their ability to learn the category "fish shape" rather than distinguishing between conspecifics and heterospecifics is discussed. The successful visual discrimination task using this complex operant conditioning device is particularly remarkable and novel for this farmed-fish species, and could be exploited to develop cognitive enrichments in future farming systems. This device can also be added to the existing repertoire of testing devices suitable for investigating cognitive abilities in fish.