Coping styles in farmed fish: consequences for aquaculture

Individual differences in physiological and behavioural responses to stressors are increasingly recognised as adaptive variation and thus raw material for evolution and fish farming improvements including selective breeding. Such individual variation has been evolutionarily conserved and is present in all vertebrate taxa including fish. In farmed animals, the interest in consistent trait associations, that is coping styles, has increased dramatically over the last years because many studies have demonstrated links to performance traits, health and disease susceptibility and welfare. This study will review (i) the main behavioural, neuroendocrine, cognitive and emotional differences between reactive and proactive coping styles in farmed fish; (ii) the methodological approaches used to identify coping styles in farmed fish, including individual (group) mass-screening tests; and (iii) how knowledge on coping styles may contribute to improved sustainability of the aquaculture industry, including welfare and performance of farmed fish. Moreover, we will suggest areas for future research, where genetic basis (heritability/epigene tic) of coping styles, and the neuroendocrine mechanisms behind consistent as well as flexible behavioural patterns are pinpointed as central themes. In addition, the ontogeny of coping styles and the influence of age, social context and environmental change in coping styles will also be discussed.European Commission under the 7th Framework Programme FP7-KBBE [265957

Stressor controllability modulates the stress response in fish

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)

Behavioural stress responses predict environmental perception in European sea bass (Dicentrarchus labrax)

Individual variation in the response to environmental challenges depends partly on innate reaction norms, partly on experience-based cognitive/emotional evaluations that individuals make of the situation. The goal of this study was to investigate whether pre-existing differences in behaviour predict the outcome of such assessment of environmental cues, using a conditioned place preference/avoidance (CPP/CPA) paradigm. A comparative vertebrate model (European sea bass, Dicentrarchus labrax) was used, and ninety juvenile individuals were initially screened for behavioural reactivity using a net restraining test. Thereafter each individual was tested in a choice tank using net chasing as aversive stimulus or exposure to familiar conspecifics as appetitive stimulus in the preferred or non preferred side respectively (called hereafter stimulation side). Locomotor behaviour (i.e. time spent, distance travelled and swimming speed in each tank side) of each individual was recorded and analysed with video software. The results showed that fish which were previously exposed to appetitive stimulus increased significantly the time spent on the stimulation side, while aversive stimulus led to a strong decrease in time spent on the stimulation side. Moreover, this study showed clearly that proactive fish were characterised by a stronger preference for the social stimulus and when placed in a putative aversive environment showed a lower physiological stress responses than reactive fish. In conclusion, this study showed for the first time in sea bass, that the CPP/CPA paradigm can be used to assess the valence (positive vs. negative) that fish attribute to different stimuli and that individual behavioural traits is predictive of how stimuli are perceived and thus of the magnitude of preference or avoidance behaviour.European Commission [265957]; Portuguese Fundacao para a Ciencia e Tecnologia (FCT) [FRH/BPD/72952/2010]; FCT [SFRH/BD/80029/2011

Development of the ultrastructure of sonic muscles: a kind of neoteny?

BACKGROUND: Drumming muscles of some sound-producing fish are ‘champions’ of contraction speed, their rate setting the fundamental frequency. In the piranha, contraction of these muscles at 150 Hz drives a sound at the same frequency. Drumming muscles of different not closely related species show evolutionary convergences. Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz. The aim of this work was to study the development of sound production and sonic and epaxial muscles simultaneously in the red bellied piranhas (Pygocentrus nattereri) to seek for possible common characteristics. RESULTS: Call, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve. In epaxial muscles, the fibre diameters of younger fish are first positioned in the graphical slope corresponding to sonic muscles, before diverging. The fibre diameter of older fish trunk muscles was bigger, and the area of the myofibrils was larger than in sonic muscles. Moreover, in two of the biggest fish, the sonic muscles were invaded by fat cells and the sonic muscle ultrastructure was similar to the epaxial one. These two fish were also unable to produce any sound, meaning they lost their ability to contract quickly. CONCLUSIONS: The volume occupied by myofibrils determines the force of contraction, the volume of sarcoplasmic reticulum sets the contraction frequency, and the volume of mitochondria sets the level of sustained performance. The functional outcomes in muscles are all attributable to shifts in the proportions of those structures. A single delay in the development restricts the quantity of myofibrils, maintains a high proportion of space in the sarcoplasm and develops sarcoplasmic reticulum. High-speed sonic muscles could thus be skeletal muscles with delayed development. This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages

Individual fish rhythm directs group feeding: a case study with sea bass juveniles (

The long term influence of individual biological rhythms on group feed demand behaviour was investigated in European sea bass (Dicentrarchus labrax) held under controlled environmental conditions with an on-demand feeding system. The experiment was realized over 219 days with 190 fish distributed on 4 tanks. Sea bass had a mean body mass comprised between 139 g to 183 g. The number of feed demand acts by each individual was calculated daily, and the population could thus be partitioned into three categories (high-, low- and zero-triggering fish). The duration of the period that an individual held high-triggering status could vary, but was 63 ± 16 days on average. The transition period between two highest-triggering fish in one tank was on average 4 ± 4 days. The group feeding rhythm followed the same pattern of feed demand rhythm as the highest-triggering individual fish. When the highest-triggering fish was nocturnal, the totality of feed demand in the group was realized during the night with one peak at 22:00, corresponding to dusk under experimental conditions. When the highest-triggering fish was diurnal, the majority of feed demand in the group was realized during the light period with one peak at 06:00, corresponding to dawn, and/or another at 12:00. This study therefore highlights that sea bass group feeding behaviour is not the sum of individual feed demand behaviours, but is directed by the rhythm and behaviour of a few high-triggering fish. The regular changes of high-triggering fish in the group proved that it was not the identity of these particular fish that was most important for the group, but their role as a feed demand leader

Assessment of sea bass swimming activity and preferential space use in sea cages using acoustic telemetry and archival tags

Swimming activity rhythms and levels as well as space occupation by sea bass, Dicentrarchus labrax, in a sea cage (6.5 x 6.5 x 8 m, ca. 25000 fish of 400 g stocked at 30 kg m-3) were recorded using acoustic telemetry (9 fish, IBDT Sonotronics) and archival tags (11, DSTs STAR ODDI). Acoustic tracking was realized over a 13 days period and successful for 3 individuals (one fix every 2 min on average). For archival tags, only 4 tags were retrieved and 3 had been recording swimming depth and temperature for 9 mo (Nov 05-June 06). Telemetry results showed an even day/night swimming activity levels in November with fish staying in close association with the bottom. Archival tags recordings revealed a preferential distribution in the water column between mid-water and bottom of the net cage in winter, over the whole water column in spring and near the surface zone in early-summer. In addition, on a 24 hrs period basis, sea bass presented a vertical movement rhythm: they swam closer to the surface during the day, specially around feeding events, and near the bottom at night. That vertical movement was pronounced during winter, faded during spring and almost disappeared in summer