A new integrative framework for the study of fish welfare based on the concepts of allostasis, appraisal and coping styles

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Publications

Are coping styles consistent in the teleost fish Sparus aurata through sexual maturation and sex reversal?

Publication . Castanheira, Maria Filipa; Martinez Paramo, S.; Figueiredo, F.; Cerqueira, Marco; Millot, Sandie; Oliveira, Catarina C. V.; Martins, Catarina I. M.; Conceicao, Luis E. C.

Individual differences in behaviour and physiological responses to stress are associated with evolutionary adaptive variation and thus raw material for evolution. In farmed animals, the interest in consistent trait associations, i.e. coping styles, has increased dramatically over the last years. However, one of limitations of the available knowledge, regarding the temporal consistency, is that it refers always to short-term consistency (usually few weeks). The present study used an escape response during a net restraining test, previously shown to be an indicative of coping styles in seabream, to investigate long-term consistency of coping styles both over time and during different life history stages. Results showed both short-term (14 days) consistency and long-term (8 months) consistency of escape response. However, we did not found consistency in the same behaviour after sexual maturation when the restraining test was repeated 16, 22 and 23 months after the first test was performed. In conclusion, this study showed consistent behaviour traits in seabream when juveniles, and a loss of this behavioural traits when adults. Therefore, these results underline that adding a life story approach to data interpretation as an essential step forward towards coping styles foreground. Furthermore, a fine-tuning of aquaculture rearing strategies to adapt to different coping strategies may need to be adjusted differently at early stages of development and adults to improve the welfare of farmed fish.

2016-10Journal article

Restricted

Stressor controllability modulates the stress response in fish

Publication . Cerqueira, Marco; Millot, Sandie; Silva, Tomé; Félix, Ana S.; Castanheira, Maria Filipa; Rey, Sonia; MacKenzie, Simon; Oliveira, Gonçalo A.; Oliveira, Catarina; Oliveira, Rui F.

Background In humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax). Results Fish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used. Conclusions These results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).

2021-08-04Journal article

Open Access

Plasticity of coping styles in farmed fish: behavioural and neuro-endocrine profiling

Publication . Castanheira, Maria Filipa Bento de Oliveira Falcão; Conceição, Luís E.C.; Martins, Catarina I. M.; Kristiansen, Tore

Intensive aquaculture practices frequently expose fish to a range of stressors. Gilthead seabream (Sparus aurata) is the most important farmed species in the Mediterranean, and like in other vertebrates, exhibit pronounced individual differences in stress responsiveness, however to which extent such variability is part of coping styles remains unclear. As such, this Thesis aimed to provide methods and tools to analyse coping styles in seabream, with specific reference to the presence, variability and consistency of individual trait correlations relevant to fish welfare. Using an evolutionary approach, it integrated and explored the adaptive links between behaviour, physiology and brain function, especially aiming to explore individual variation in adaptive responses of seabream when exposed to the same stressful situation. The background and consequences of coping styles in aquaculture is introduced in Chapter 2. Chapter 3 aims to quantify individual differences in cortisol response in seabream and to assess whether it can predict aggressive behaviour. Results provided the first evidence for a link between HPI responsiveness and aggressive behaviour in seabream. This suggests that individual differences in aggression are part of coping styles and therefore can be predictive of and predicted from other traits. In Chapter 4, it was investigated, for the first time in seabream, whether individual differences in behavioural responses to a variety of challenges are consistent over time and across contexts using both individual and grouped-based tests. Results suggest consistency over time and across-context in behavioural responses to challenges both using individual and grouped-based tests. This study highlights the possibility to predict behaviour in groups from individual coping traits. One of the traits that has been shown to be consistent over time and across context in the Chapter 4 was the escape response under a restraining test. Using this trait as a proxy of coping styles in seabream the consistency of escape behaviour was investigated in Chapter 5 and 6. In Chapter 5 we investigated the effect of avoidance in gilthead seabream kept under different social contexts, i.e. the influence of other group members on individual avoidance behaviour consistency. The results demonstrate that grouping individuals with similar coping styles induces changes in coping styles whereas grouping individuals with different coping styles favours coping styles to remain the same. These findings suggest an influence of the social environment in seabream coping styles. In Chapter 6 we investigate the long term consistency of coping styles both, over time and during different life history stages. Our results show consistent behaviour traits in seabream when juveniles, and a loss of these behavioural traits when adults. Therefore, these results underline that adding a life history approach to data interpretation is as an essential step forward towards understanding coping styles. Chapter 7 aimed to characterize the stress coping ability and brain function in seabream, by investigating the behavioural and forebrain physiological responses of fish displaying contrasting coping styles to the same stimulus (escape response under a restraining test). Results show differences in activation of region-specific telencephalic regions between seabream displaying contrasting coping styles. It confirms the hypothesis that in seabream, inhibitory and excitatory markers of neural function appear to be associated with reactive and proactive coping styles, respectively. The main findings of this thesis are discussed and the main conclusions are presented in Chapter 8. It is concluded that fish with contrasting stress coping styles show clear differences in behavioural and physiological parameters. Moreover, these differences can change according to social environment and life history. In general this Thesis has generated new knowledge of the mechanisms underlying individual responses of fish to stress providing new insights on the interrelations between different relevant husbandry practices, fish performance and welfare.

2016-07-22Doctoral thesis

Open Access

Can we predict personality in fish? searching for consistency over time and across contexts

Publication . Castanheira, Maria Filipa; Herrera, Marcelino; Costas, Benjamin; Conceicao, Luis E. C.; Martins, Catarina I. M.

The interest in animal personality, broadly defined as consistency of individual behavioural traits over time and across contexts, has increased dramatically over the last years. Individual differences in behaviour are no longer recognised as noise around a mean but rather as adaptive variation and thus, essentially, raw material for evolution. Animal personality has been considered evolutionary conserved and has been shown to be present in all vertebrates including fish. Despite the importance of evolutionary and comparative aspects in this field, few studies have actually documented consistency across situations in fish. In addition, most studies are done with individually housed fish which may pose additional challenges when interpreting data from social species. Here, we investigate, for the first time in fish, whether individual differences in behavioural responses to a variety of challenges are consistent over time and across contexts using both individual and grouped-based tests. Twenty-four juveniles of Gilthead seabream Sparus aurata were subjected to three individual-based tests: feed intake recovery in a novel environment, novel object and restraining and to two group-based tests: risk-taking and hypoxia. Each test was repeated twice to assess consistency of behavioural responses over time. Risk taking and escape behaviours during restraining were shown to be significantly consistent over time. In addition, consistency across contexts was also observed: individuals that took longer to recover feed intake after transfer into a novel environment exhibited higher escape attempts during a restraining test and escaped faster from hypoxia conditions. These results highlight the possibility to predict behaviour in groups from individual personality traits.

2013-04Journal article

Open Access

Cognitive appraisal of environmental stimuli induces emotion-like states in fish

Publication . Cerqueira, M.; Millot, S.; Castanheira, Maria Filipa; Félix, Ana Sofia; Silva, T.; Oliveira, Gonçalo; Oliveira, C. C.; Martins, C. I. M.; Oliveira, Rui F.

The occurrence of emotions in non-human animals has been the focus of debate over the years. Recently, an interest in expanding this debate to non-tetrapod vertebrates and to invertebrates has emerged. Within vertebrates, the study of emotion in teleosts is particularly interesting since they represent a divergent evolutionary radiation from that of tetrapods, and thus they provide an insight into the evolution of the biological mechanisms of emotion. We report that Sea Bream exposed to stimuli that vary according to valence (positive, negative) and salience (predictable, unpredictable) exhibit different behavioural, physiological and neuromolecular states. Since according to the dimensional theory of emotion valence and salience define a two-dimensional affective space, our data can be interpreted as evidence for the occurrence of distinctive affective states in fish corresponding to each the four quadrants of the core affective space. Moreover, the fact that the same stimuli presented in a predictable vs. unpredictable way elicited different behavioural, physiological and neuromolecular states, suggests that stimulus appraisal by the individual, rather than an intrinsic characteristic of the stimulus, has triggered the observed responses. Therefore, our data supports the occurrence of emotion-like states in fish that are regulated by the individual's perception of environmental stimuli.

2017-10Journal article

Open Access