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- Are personality traits consistent in fish? The influence of social contextPublication . Castanheira, Maria Filipa; Cerqueira, Marco; Millot, Sandie; Gonçalves, Rui A.; Oliveira, Catarina C. V.; Conceição, Luis E. C.; Martins, Catarina I. M.Individual differences in behavioural and physiological responses to challenges are progressively accepted as adaptive variation and reveal a strong degree of evolutionary conservation throughout the vertebrate taxa. Previous studies in gilthead seabream (Sparus aurata) suggested that individual differences in behaviour reflect distinct coping styles or personality, contrasting consistent traits associations. One of the traits that have been shown to be consistent over time and across context is the escape response under a restraining test. Using this trait as a proxy of personality in seabream the influence of social context in the consistency of escape behaviour was investigated. Individually tagged juvenile seabream (n = 360; 70.18 +/- 11.44 g; mean +/- SD) were subjected to a restraining test that consisted of keeping each fish in an emerged net for one minute. Behaviours measured in the net (latency to escape; number of escape attempts and total time spent on escaping) were collapsed into first principal component scores using Principal Components Analysis (PCA). Using the PCA scores the individuals were distributed into homogeneous groups (n = 30 each group) of proactive, reactive and intermediate. Control groups consisted of mixed groups with 1/3 of each coping style. After one month the same individuals were exposed to the same test (restraining test) to assess consistency of behavioural responses. Results indicate that homogenous groups of proactive (p = 0.086) and reactive (p = 0.159) individuals did not exhibit consistent behavioural responses as opposed to the intermediate (p = 0.028) and control groups (p < 0.001). This study thus confirms that the social context in which fish are kept significantly influence personality traits. (C) 2016 Elsevier B.V. All rights reserved.
- Daily oxygen consumption rhythms of Senegalese sole solea senegalensis (Kaup, 1858) juvenilesPublication . Castanheira, Maria Filipa; Martins, C. I. M.; Engrola, S.; Conceição, L. E. C.Senegalese sole is known to be a species with pronounced nocturnal feeding behaviour. However, as for most fish species, there is a lack of knowledge concerning the influence of such biological rhythmon metabolic rate. The aim of this study was to determine whether individual variation in routine and fed metabolic rate was affected by daily light–dark rhythms in juveniles of Senegalese sole. The individual oxygen consumption measurements in Senegalese sole juveniles were determined by flow-through respirometry, at fasted conditions and after the fish were fed a single meal, the meal time started at 0930 h and fish fed ad libitum for 30 min. The measurements were made during 22 h, of which 8 h was in the light and 14 h in the dark, and started immediately after transfer to the respiratory chambers at 1100 h. The results suggest an influence of light–dark cycles in routine metabolism. It was observed that oxygen consumption increased during the dark phase in fasted fish (FAST) but was higher during the light phase in fed fish (FEED). However, when feed is provided during the light phase, juveniles are capable of shifting oxygen consumption rhythms to respond to the energetic demands of digestion and growth. These results suggest that routine metabolism varies according to the species natural habits as Senegalese sole is known to be nocturnal. The findings of this study underline the importance of understanding the biological rhythms of the species under study before metabolic data are interpreted.
- Effect of varying dietary levels of LC-PUFA and vegetable oil sources on performance and fatty acids of Senegalese sole post larvae: Puzzling results suggest complete biosynthesis pathway from C18 PUFA to DHAPublication . Navarro-Guillén, Carmen; Engrola, S.; Castanheira, Maria Filipa; Bandarra, N.; Hachero-Cruzado, Ismael; Tocher, Douglas R.; Conceição, L. E. C.; Morais, S.Lipid nutrition of marine fish larvae has focused on supplying essential fatty acids (EFA) at high levels to meet requirements for survival, growth and development. However, some deleterious effects have been reported suggesting that excessive supply of EFA might result in insufficient supply of energy substrates, particularly in species with lower EFA requirements such as Senegalese sole (Solea senegalensis). This study addressed how the balance between EFA and non-EFA (better energy sources) affects larval performance, body composition and metabolism and retention of DHA, by formulating enrichment emulsions containing two different vegetable oil sources (olive oil or soybean oil) and three DHA levels. DHA positively affected growth and survival, independent of oil source, confirming that for sole post-larvae it is advantageous to base enrichments on vegetable oils supplying higher levels of energy, and supplement these with a DHA-rich oil. In addition, body DHA levels were generally comparable considering the large differences in their dietary supply, suggesting that the previously reported ∆4 fatty acyl desaturase (fad) operates in vivo and that DHA was synthesized at physiologically significant rates through a mechanism involving transcriptional up-regulation of ∆4fad, which was significantly up-regulated in the low DHA treatments. Furthermore, data suggested that DHA biosynthesis may be regulated by an interaction between dietary n − 3 and n − 6 PUFA, as well as by levels of LC-PUFA, and this may, under certain nutritional conditions, lead to DHA production from C18 precursors. The molecular basis of putative fatty acyl ∆5 and ∆6 desaturation activities remains to be fully determined as thorough searches have found only a single (∆4) Fads2-type transcript. Therefore, further studies are required but this might represent a unique activity described within vertebrate fads.
- 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.
- Addressing the welfare needs of farmed lumpfish: knowledge gaps, challenges and solutionsPublication . Garcia de Leaniz, Carlos; Gutierrez Rabadan, Carolina; Barrento, Sara I.; Stringwell, Rebecca; Howes, Paul N.; Whittaker, Ben A.; Minett, Jessica F.; Smith, Robert G.; Pooley, Craig L.; Overland, Ben J.; Biddiscombe, Leigh; Lloyd, Richard; Consuegra, Sofia; Maddocks, Jake K.; Deacon, Paul T. J.; Jennings, Ben T.; Rey Planellas, Sonia; Deakin, Amanda; Moore, Amber I.; Phillips, Daniel.; Bardera, Guillermo; Castanheira, Maria Filipa; Scolamacchia, Maria; Clarke, Nancy; Parker, Ollie; Avizienius, John; Johnstone, Malcolm; Pavlidis, MichalisLumpfish (Cyclopterus lumpus L.) are increasingly being used as cleaner fish to control parasitic sea lice, one of the most important threats to salmon farming. However, lumpfish cannot survive feeding solely on sea lice, and their mortality in salmon net pens can be high, which has welfare, ethical and economic implications. The industry is under increasing pressure to improve the welfare of lumpfish, but little guidance exists on how this can be achieved. We undertook a knowledge gap and prioritisa tion exercise using a Delphi approach with participants from the fish farming sector, animal welfare, academia and regulators to assess consensus on the main challenges and potential solutions for improving lumpfish welfare. Consensus among participants on the utility of 5 behavioural and 12 physical welfare indicators was high (87–89%), reliable (Cronbach's alpha = 0.79, 95CI = 0.69–0.92) and independent of participant background. Participants highlighted fin erosion and body damage as the most use ful and practical operational welfare indicators, and blood parameters and behav ioural indicators as the least practical. Species profiling revealed profound differences between Atlantic salmon and lumpfish in relation to behaviour, habitat preferences, nutritional needs and response to stress, suggesting that applying a common set of welfare standards to both species cohabiting in salmon net-pens may not work well for lumpfish. Our study offers 16 practical solutions for improving the welfare of lumpfish and illustrates the merits of the Delphi approach for achieving consensus among stakeholders on welfare needs, targeting research where is most needed and generating workable solutions.
- A global assessment of welfare in farmed fishes: the FishEthoBasePublication . Saraiva, João; Arechavala Lopez, Pablo; Castanheira, Maria Filipa; Volstorf, Jenny; Heinzpeter Studer, BilloFish welfare is an essential issue that needs to be tackled by the aquaculture industry. In order to address it, studies have been limited to a small number of species and the information is generally scattered. In order to have a consistent overview of the welfare of farmed fishes, we present the FishEthoBase, an open-access database that ultimately aims to provide information on the welfare of all fish species currently farmed worldwide. Presently with 41 species, this database is directed to all stakeholders in the field and targets not only to bridge the gaps between them but also to provide scientific information to improve the welfare of fish. The current text explains the database and presents an analysis of the welfare scores of 41 species, suggesting that (i) the general welfare state of farmed fishes is poor, (ii) there is some potential for improvement and (iii) this potential is related to research on species’ needs, but (iv) there are many remaining knowledge gaps and (v) current fish farming technologies do not seem to fully address welfare issues. The existence of a framework, such as the FishEthoBase, is proposed as fundamental to the design of strategies that improve the welfare of farmed fish.
- Can we predict personality in fish? searching for consistency over time and across contextsPublication . 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.
- Plasticity of coping styles in farmed fish: behavioural and neuro-endocrine profilingPublication . Castanheira, Maria Filipa Bento de Oliveira Falcão; Conceição, Luís E.C.; Martins, Catarina I. M.; Kristiansen, ToreIntensive 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.
- Metabolic basis of growth variation in juvenile sole (Solea senegalensis, Kaup 1858)Publication . Castanheira, Maria Filipa Bento de Oliveira Falcão; Conceição, L. E. C.; Engrola, S.The general aim of this study was to understand the underlying factors responsible for the individual variation in growth of juvenile Senegalese sole (Solea senegalensis). Senegalese sole is a species of high commercial value and high interest for aquaculture in Europe, therefore it would be important to understand these individual variations. Understanding the causes for individual variation in growth in relation with the feed intake, metabolic rate and response to stress contributes to maximize the production efficiency by reducing food waste and improving water quality. In order to identify the possible factors responsible for the individual variation in sole growth, its relationship with metabolic rate, stress response and feed intake was determined. Twelve fish with 18.49 ± 2.94g of initial weight were kept in standard conditions and feed once a day, during a period of six months. Individual oxygen consumption measurements in Sole juveniles were determined by flow-through respirometry at standard conditions, after the fish were fed a single meal and after a stressful condition. Blood samples for plasma cortisol, were taken from all fish at the start of the experiment (control, indicative of basal levels) and after stress exposure. Quantification of individual feed intake was performed by incorporation with radio-opaque ballotinis glass beads in a dry feed, followed by radiography to quantify the amount of ingested pellets. Individual fish exhibited pronounced variation in growth (final weight ranging from 30.45 to 67.53g), oxygen consumption of fasted fish (108.0 to 447.4 μmol/g/h), oxygen consumption of fed fish (174.7 μmol/g/h to 813.5 μmol/g/h), oxygen consumption after emersion stress (186.8 μmol/g/h to 376.7 μmol/g/h), and plasma cortisol after emersion stress (4.81 ng/ml to 46.45 ng/ml). Individual differences in metabolic rate do not contribute to explain individual differences in growth. However, after emersion stress individual differences in stress response seem to play a role in explaining individual differences in growth, what may result from different copying styles. Sole feed intake as measured by X-ray does not seem to be a good indicator of growth rate. The oxygen consumption increases both when fish are fed and after an emersion stress, as result of additive costs of growth and stress to the cost of maintenance. All together, this study suggests that individual variation of growth in Solea senegalensis is essentially due to genetic variation, and its reduction may accomplished when genetic selection programs are adopted. Furthermore, a study with a larger number of fish and over a larger time period would be important to check some of the trends found in this thesis between growth potential, metabolic rate and coping styles of Senegalese sole.
- Cognitive appraisal of environmental stimuli induces emotion-like states in fishPublication . 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.