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

Abstract

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.

Figure 1

Median (quartiles: 25%, 75%) percentage of fish group activity (% of differing pixels between two successive images) on (A) day 1 and on (B) day 12 of conditioning. Activity is measured in the bubble area during the 15 s of bubbles until the 5 s of time gap after bubbles for all treatments, corresponding to the period before the expected feeding for treatments BUBBLE + TIME and BUBBLE (total analysis duration of 20 s). The black point inside boxes represents the mean value (Tukey post-hoc tests).

Figure 2

Median (quartiles: 25%, 75%) percentage of fish group activity (% of differing pixels between two successive images) in the bubble area on the day 12 of conditioning. “During bubbles” represents the 15 s of bubble diffusion + 5 s of time gap for all treatments. “Neutral period” represents 6-min periods with no feed delivery or bubble diffusion. The black point inside boxes represents the mean value (Tukey post-hoc test).

Figure 3

Median (quartiles: 25%, 75%) percentage of fish group activity (% of differing pixels between two successive images) in the whole tank during the 6-min period preceding feed delivery. Results are given for each treatment and for the three feedings on (A) day 1 and (B) day 12 of conditioning. F1, F2 and F3 correspond to the three feedings analysed. The black point inside boxes represents the mean value. Different latin letters indicate significant differences between treatments, and different greek letters indicate differences between feedings (P < 0.05; Tukey post-hoc tests).

Figure 4

Median (quartiles: 25%, 75%) number of agonistic behaviours, burst of accelerations, and jumps scored per minute in the whole tank over 6 min preceding feed delivery in the four treatments. The black point inside boxes represents the mean value. Different letters indicate significant differences between treatments (P < 0.05; Tukey post-hoc tests).

Figure 5

Median (quartiles: 25%, 75%) percentage of fish group activity (% of differing pixels between two successive images) during feed omissions. Activity is measured in the bubble area during bubble diffusion to 30 s after bubbles (total analysis duration of 45 s: 15 s of bubbles, the 5 s of time gap before the expected feeding for treatments BUBBLE + TIME and BUBBLE, and 25 s after the omission. For treatments TIME and RANDOM, the period of 25 s started 5 s after the end of bubbles). The black point inside boxes represents the mean value. Different letters indicate significant differences between treatments (P < 0.05; Tukey post-hoc tests).

Figure 6

Median (quartiles: 25%, 75%) number of agonistic behaviours, burst of accelerations, and jumps scored per minute during (A) the 6-min period following each of the three feed omission occasions, when pooled, and (B) three neutral periods of 6 min free from feedings or bubbles on day 12. The black point inside boxes represents the mean value. Different letters indicate significant differences between treatments (P < 0.05; Tukey post-hoc tests).

Figure 7

(A) General schedule of the experiment with a first period of acclimatation to the environment, the conditioning involving the four different predictability conditions of feeding between day 1 and day 12, then the three feed omissions performed in all treatments, and the novel tank-test after which growth parameters were recorded; (B) Example of a day during conditioning for each treatment, with BUBBLE + TIME based on temporal + signalled predictability of feeding (based on time and bubble diffusion), BUBBLE based on signalled predictability alone (based on bubble diffusion), TIME based on temporal predictability alone (based on time of day), and RANDOM corresponding to unpredictable feedings (random feeding delivery). B1 to B5 represent the five daily bubble diffusions, and F1 to F5 the five daily feedings; (C) Areas used for fish behaviour analyses (on the left: the bubble area where bubbles were diffused; on the right: the whole tank).