Unexpected appetitive events promote positive affective state in juvenile European sea bass

Abstract

Some animal species exhibit considerable physiological and behavioural alterations in response to captivity. It has been hypothesized, but rarely tested, that such changes reflect a negative affective state that is associated to this specific context. In the last years, judgement bias measures have emerged as reliable indicators of animal affective state, under the assumption that individuals in a negative affective state are more likely to evaluate ambiguous stimuli as negative and display therefore pessimistic behaviours. Here, we have developed a judgement bias task for juvenile European sea bass (Dicentrarchus labrax) aiming to measure optimism/pessimism in this marine species, which have previously been reported to show important dysregulations in captive settings. Our results show that juvenile sea bass exhibit a considerable bias towards pessimistic behaviours in laboratory settings. Furthermore, juveniles that received an unexpected positive event during the judgement bias test displayed more optimistic responses toward ambiguous stimuli as compared to control fish, indicating a positive change in their affective state induced by the appetitive experience. These results reveal a direct interaction of the internal affective state with decision-making processing under ambiguity in juvenile European sea bass, highlighting therefore the potential of judgement bias tests as a tool for the advancement and improvement of our understanding of welfare in finfish aquaculture.

Figure 1

Behavioral characterization of judgement bias in juvenile European sea bass. (A) Diagram of the half radial maze highlighting the two reference arms (positive/rewarded (P; social reward/ exposure to a conspecific) and negative/aversive (N; punishment/ chasing with a net)) that were used in the judgement bias test (JBT) for juvenile sea bass. Once juveniles are able to discriminate between P and N arms, only their responses to an ambiguous arm—which is located midway between the two reference arms (90°) and contains a mixed coloured card (1:1)—were tested. (B) Illustration of the combination of the frequency distribution of the judgement bias score (JBS) among juveniles that completed the judgement bias task (n = 43) with the Kernel density estimation, which calculates the probability density of JBS. Drawing of diagram in (A) by Iara Chapuis.

Figure 2

Behavioral differences between optimistic and pessimistic juveniles (n = 11 and n = 32, respectively) in the open field test with shelter (OFT): (A) Diagram of the OFT; (B) latency to leave the shelter for the first time (s); (C) number of times leaving the shelter; and (D) time spent outside the shelter (s). Asterisks indicate significant differences between experimental groups. Drawing of diagram in (A) by Iara Chapuis.

Figure 3

Behavioral differences between optimistic and pessimistic juveniles (n = 11 and n = 32, respectively) in the novel object test (NOT): (A) Diagram of the NOT; (B) number of approaches to the novel object; (C) time spent in the novel object zone (s); (D) distance from the novel object (cm); (E) latency to first approach to the novel object (s); (F) angular velocity (deg/s); and (G) time in freezing (s). Asterisks indicate significant differences between experimental groups. Drawing of diagram in (A) by Iara Chapuis.

Figure 4

Effects of unexpected appetitive experiences on decision-making under ambiguity. (A) Performance of juvenile sea bass receiving or not pretest positive experience (specimen of Gammarus) in the judgement bias paradigm (n = 12–15 per experimental group: control and unexpected positive event). Different letters indicate significant differences between the experimental groups for each stimulus (P, N, A) following planned comparisons tests. Data are expressed as mean ± s.e.m.; (B) JBS of juvenile sea bass receiving or not pretest positive experience (n = 12–15 per experimental group: no pretest positive event, and pretest positive event). Asterisks indicate significant differences between experimental groups; (C) Response of juvenile sea bass receiving or not pretest experience (specimen of fresh frozen Gammarus pulex) to a novel stimulus (n = 9 per experimental group: control and unexpected positive event). Drawing of Gammarus in (A) and (B) by Iara Chapuis.