How to measure exploration: A combined estimation method.

The personality axis 'exploration-avoidance' is often measured using an open field test (OFT) from which measurements such as mobility level (e.g. distance travelled) and space use (e.g. area covered) in an unknown environment are extracted. Recently developed tracking software surprisingly includes only a measure of mobility level in their output summary. Consequently, recent articles using these software programs started to ignore a measure of space use in their determination of exploration. In this short communication, we show briefly why it is important to not overlook a measure of space use, provide an easy way to calculate such a measure, with adjustable resolution, from the available position data provided by the software and a method to determine a proxy for exploration.

Variation in personality shaped by evolutionary history, genotype and developmental plasticity in response to feeding modalities in the Arctic charr.

Animal personality has been shown to be influenced by both genetic and environmental factors and shaped by natural selection. Currently, little is known about mechanisms influencing the development of personality traits. This study examines the extent to which personality development is genetically influenced and/or environmentally responsive (plastic). We also investigated the role of evolutionary history, assessing whether personality traits could be canalized along a genetic and ecological divergence gradient. We tested the plastic potential of boldness in juveniles of five Icelandic Arctic charr morphs (Salvelinus alpinus), including two pairs of sympatric morphs, displaying various degrees of genetic and ecological divergence from the ancestral anadromous charr, split between treatments mimicking benthic versus pelagic feeding modalities. We show that differences in mean boldness are mostly affected by genetics. While the benthic treatment led to bolder individuals overall, the environmental effect was rather weak, suggesting that boldness lies under strong genetic influence with reduced plastic potential. Finally, we found hints of differences by morphs in boldness canalization through reduced variance and plasticity, and higher consistency in boldness within morphs. These findings provide new insights on how behavioural development may impact adaptive diversification.

Enhancement of Soybean Meal Alters Gut Microbiome and Influences Behavior of Farmed Atlantic Salmon (Salmo salar).

Atlantic salmon (Salmo salar) is one of the worlds most domesticated fish. As production volumes increase, access to high quality and sustainable protein sources for formulated feeds of this carnivorous fish is required. Soybean meal (SBM) and soy-derived proteins are the dominant protein sources in commercial aquafeeds due to their low-cost, availability and favorable amino acid profile. However, for Atlantic salmon, the inclusion of soybean meal (SBM), and soy protein concentrate (SPC) in certain combinations can impact gut health, which has consequences for immunity and welfare, limiting the use of soy products in salmonid feeds. This study sought to address this challenge by evaluating two gut health-targeted enhancements of SBM for inclusion in freshwater phase salmon diets: enzyme pre-treatment (ETS), and addition of fructose oligosaccharide (USP). These were compared with untreated soybean meal (US) and fish meal (FM). This study took a multi-disciplinary approach, investigating the effect on growth performance, gut microbiome, and behaviors relevant to welfare in aquaculture. This study suggests that both enhancements of SBM provide benefits for growth performance compared with conventional SBM. Both SBM treatments altered fish gut microbiomes and in the case of ETS, increased the presence of the lactic acid bacteria Enterococcus. For the first time, the effects of marine protein sources and plant protein sources on the coping style of salmon were demonstrated. Fish fed SBM showed a tendency for more reactive behavior compared with those fed the FM-based control. All fish had a similar low response to elicited stress, although ETS-fed fish responded more actively than US-fed fish for a single swimming measure. Furthermore, SBM-fed fish displayed lower repeatability of behavior, which may indicate diminished welfare for intensively farmed fish. The implications of these findings for commercial salmonid aquaculture are discussed.

Personality in juvenile Atlantic cod ecotypes and implications for fisheries management.

Animals show among-individual variation in behaviors, including migration behaviors, which are often repeatable across time periods and contexts, commonly termed "personality." These behaviors can be correlated, forming a behavioral syndrome. In this study, we assessed the repeatability and correlation of different behavioral traits, i.e., boldness, exploration, and sociality, and the link to feeding migration patterns in Atlantic cod juveniles. To do so, we collected repeated measurements within two short-term (3 days) and two long-term (2 months) intervals of these personality traits and genotypes of the Pan I locus, which is correlated with feeding migration patterns in this species. We found high repeatabilities for exploration behavior in the short- and long-term intervals, and a trend for the relationship between exploration and the Pan I locus. Boldness and sociality were only repeatable in the second short-term interval indicating a possible development of stability over time and did not show a relation with the Pan I locus. We found no indication of behavioral syndromes among the studied traits. We were unable to identify the existence of a migration syndrome for the frontal genotype, which is the reason that the link between personality and migration remains inconclusive, but we demonstrated a possible link between exploration and the Pan I genotype. This supports the need for further research that should focus on the effect of exploration tendency and other personality traits on cod movement, including the migratory (frontal) ecotype to develop management strategies based on behavioral units, rather than treating the population as a single homogeneous stock.

Activity vs exploration: Locomotion in a known and unknown environment differs in Atlantic cod juveniles (Gadus morhua).

Individuals within a population often behave differently and these differences can be consistent over time and/or context, also termed "animal personality". Animal personality has been commonly classified into five axes with studies aiming to validate these axes. One subject that has surprisingly not received full attention yet is the difference between the two personality axes "activity" and "exploration-avoidance", i.e. behaviour in a known vs an unknown environment. Despite this clear difference in definition, many studies measure activity in an unknown environment and term it activity, while underlying motivations between the two environments are different. This study aimed to detect the two personality traits "activity" and "exploration" in Atlantic cod juveniles, and to investigate whether they support the distinctive definitions proposed by previous authors. This study showed significant consistency in locomotion variation in both environments, i.e. personality. In addition, the two environments clearly elicited different behaviours; Atlantic cod juvenile behaviour was more repeatable and they moved more in the known vs the unknown environment, and no correlation of the proportional locomotion between the two was found. This demonstrates that locomotion in both environments, i.e. the personality axes "activity" and "exploration", should not be confused nor treated as if they reflect the same personality trait.

Torula yeast in the diet of Atlantic salmon Salmo salar and the impact on growth performance and gut microbiome.

Atlantic salmon aquaculture is expanding, and with it, the need to find suitable replacements for conventional protein sources used in formulated feeds. Torula yeast (Cyberlindnera jadinii), has been identified as a promising alternative protein for feed and can be sustainably cultivated on lignocellulosic biomasses. The present study investigated the impact of torula yeast on the growth performance and gut microbiome of freshwater Atlantic salmon. A marine protein base diet and a mixed marine and plant protein base diet were tested, where conventional proteins were replaced with increasing inclusion levels of torula yeast, (0%, 10%, 20%). This study demonstrated that 20% torula yeast can replace fish meal without alteration to growth performance while leading to potential benefits for the gut microbiome by increasing the presence of bacteria positively associated with the host. However, when torula yeast replaced plant meal in a mixed protein diet, results suggested that 10% inclusion of yeast produced the best growth performance results but at the 20% inclusion level of yeast, potentially negative changes were observed in the gut microbial community, such as a decrease in lactic acid bacteria. This study supports the continued investigation of torula yeast for Atlantic salmon as a partial replacement for conventional proteins.

The effect of ultrasonic antifouling control on the growth and microbiota of farmed European sea bass (Dicentrarchus labrax).

Biofouling is a serious threat to marine renewable energy structures and marine aquaculture operations alike. As an alternative to toxic surface coatings, ultrasonic antifouling control has been proposed as an environmentally friendly means to reduce biofouling. However, the impact of ultrasound on fish farmed in offshore structures or in marine multi-purpose platforms, combining renewable energy production and aquaculture, has not yet been assessed. Here we study the impact of ultrasound on the growth and microbiota of farmed European sea bass (Dicentrarchus labrax) under laboratory conditions. Whereas growth and survival were not reduced by ultrasound exposure, microbiological analysis using plate counts and 16S rRNA gene based metataxonomics showed a perturbation of the gill and skin microbiota, including an increase in putative pathogenic bacteria. This warrants further research into the long-term effects of ultrasonic antifouling control on the health and wellbeing of farmed fish.

Marine aggregates in North Atlantic coast: Microbial characteristics and potential interactions with farmed Atlantic salmon (Salmo salar).

Microbial contamination of aggregates collected near an Atlantic salmon farm, in the Cherbourg roadstead, was followed monthly over one year to study the dynamics of Vibrio spp. and explore their impact on farmed fish. Salmon state of health was followed through blood and histopathological analyses. Vibrio were systematically found in aggregates with particularly high concentration in August. The Splendidus clade was strongly dominant in aggregates as well as in gills, and an increase in Vibrio diversity was observed in summer and autumn. Results did not demonstrate that aggregates directly impact the bacterial community of gills, but they suggested an aggregates-gills interaction. Gill contamination was correlated with water temperature and probably impacted by amoebae. Vibrio renipiscarius and Vibrio toranzoniae were isolated in North Atlantic for the first time. A better understanding of the interaction between marine aggregates, Vibrio spp. and fish is essential to improve salmon cage farming.

Relationship between individual and group learning in a marine teleost: A case study with sea bass under self-feeding conditions.

Fish learning and cognition are usually approached by testing single individuals in various devices such as mazes that have serious drawbacks, especially in gregarious species, including the stress induced by the test procedure. This might impair the results and lead to misinterpretation about the learning abilities of the targeted species. In order to provide an alternative to the individual-based tests, we investigated for the first time the operant conditioning of four similar groups (50 individuals per tank) of sea bass. We used two computerized self-feeder devices per tank, each coupled with individual electronic identification and that were alternately activated during varying positive appetitive reinforcement period of time (7 to 1 day). Learning abilities were examined at both group and individual levels. At the group level, the operant conditioning was demonstrated as the triggering activity significantly decreased when the device was turned off and increased when it was turned on, whatever the reinforcement period duration. The individual level analysis revealed a more complex situation with fish showing different learning performances that can be best explained through the producer-scrounger game theory.

Heritability of Boldness and Hypoxia Avoidance in European Seabass, Dicentrarchus labrax.

To understand the genetic basis of coping style in European seabass, fish from a full factorial mating (10 females x 50 males) were reared in common garden and individually tagged. Individuals coping style was characterized through behavior tests at four different ages, categorizing fish into proactive or reactive: a hypoxia avoidance test (at 255 days post hatching, dph) and 3 risk-taking tests (at 276, 286 and 304 dph). We observed significant heritability of the coping style, higher for the average of risk-taking scores (h2 = 0.45 ± 0.14) than for the hypoxia avoidance test (h2 = 0.19 ± 0.10). The genetic correlations between the three risk-taking scores were very high (rA = 0.96-0.99) showing that although their repeatability was moderately high (rP = 0.64-0.72), successive risk-taking tests evaluated the same genetic variation. A mild genetic correlation between the results of the hypoxia avoidance test and the average of risk-taking scores (0.45 ± 0.27) suggested that hypoxia avoidance and risk-taking tests do not address exactly the same behavioral and physiological responses. Genetic correlations between weight and risk taking traits showed negative values whatever the test used in our population i.e. reactive individual weights were larger. The results of this quantitative genetic analysis suggest a potential for the development of selection programs based on coping styles that could increase seabass welfare without altering growth performances. Overall, it also contributes to a better understanding of the origin and the significance of individual behavioral differences.

The shy prefer familiar congeners.

The shy-bold continuum is both a fundamental aspect of human behavior and a relatively stable behavioral trait for many other species. Here we assessed whether shy individuals prefer familiar congeners, taking the European sea bass, a recently domesticated fish showing similar behavioral responses to wild fish, as a model to better understand the inter-individual variability in social behavior previously observed in this species. In the wild, the link between familiarity i.e., the preference of fish for familiar congeners and boldness could be part of the mechanism underlying shoaling formation in fish. Thirty fish were individually tested in a device designed to assess the preference for a familiar vs. an unfamiliar congener on the basis of visual cues only. An open field test (OFT) with shelter was performed on the same fish 32 days later to assess the boldness of each individual. Variables of interest included the proportion of time spent in the shelter, border and center zone of the arena and variables of activity. Variables measured in OFT were collapsed into first principal component scores using Principal Components Analysis (PCA) which allowed characterizing a shy-bold continuum. Time spent near the familiar congener was negatively correlated with boldness i.e., shy individuals spent most of the time near the familiar congener. We discuss the relevance of these findings to the understanding of the behavior of European sea bass and suggest that the link between familiarity and shyness is a general aspect of both animal and human behavior.

First Insight into Exploration and Cognition in Wild Caught and Domesticated Sea Bass (Dicentrarchus labrax) in a Maze.

European sea bass aquaculture is so recent that very little is known on the effects of the early steps of its domestication. Behavioural parameters are sensitive indicators of the domestication process since they are generally impacted as soon as the first generation. The present work compared wild-caught and domesticated sea bass juvenile swimming activity, exploration and ability to learn to discriminate between two 2-D objects associated to a simple spatial task that enabled the tested individual to visually interact with an unfamiliar congener (the reward) located behind a transparent wall at the end of one of the two arms of a maze. Ten fish from each origin were individually tested 3 times in a row during 3 days (9 trials in total). Fish were placed in a start box closed by a transparent wall located in front of two 2-D objects. Fish were filmed during 10 min after the removal of the start box wall. Different swimming variables including angular velocity, total distance travelled and velocity mean, were analyzed from videos as well as the time spent in each of 6 virtual zones including the reward zone near the congener (Cong) and the zone opposite to the reward zone (OpCong). Two learning criteria were chosen: the number of successful turns and time to reach Cong. Behavioural differences were found between domesticated and wild fish. Angular velocity was higher in wild fish while the distance travelled and the velocity mean were higher in domesticated ones. Wild and domesticated fish spent most of the time in Cong and in OpCong. No differences were seen in learning ability between wild and domesticated fish. However, our findings for learning require confirmation by further studies with larger numbers of learning sessions and experiments designed to minimise stress. This study therefore demonstrated an impact of domestication on swimming behaviour but not on spatial learning.