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Summary1. Individuals of the same species often exhibit consistent differences in metabolic rate, but the effects of such differences on ecologically important behaviours remain largely unknown. In particular, it is unclear whether there is a cause-and-effect relationship between metabolic rate and the tendency to take risks while foraging. Individuals with higher metabolic rates may need to take greater risks while foraging to obtain the additional food required to satisfy their energy requirements. Such a relationship could be exacerbated by food deprivation if a higher metabolic demand also causes greater mass loss and hunger. 2. We investigated relationships among metabolic rate, risk-taking and tolerance of food deprivation in juvenile European sea bass. Individual fish were tested for risk-taking behaviours following a simulated predator attack, both before and after a 7-day period of food deprivation. The results were then related to their routine metabolic rate (RMR), which was measured throughout the period of food deprivation. 3. The amount of risk displayed by individual fish before food deprivation showed no relationship with RMR. After food deprivation, however, the amount of risk among individuals was positively correlated with RMR. In general, most fish showed an increase in risk-taking after food deprivation, and the magnitude of the increase in risk-taking was correlated with the rate of individual mass loss during food deprivation, which was itself strongly correlated with RMR. 4. The observation that RMR was related to risk-taking behaviour after food deprivation, but not before, suggests that although RMR can influence risk-taking, the strength of the relationship is flexible and context dependent. The effects of RMR on risk-taking may be subtle or non-existent in regularly feeding animals, but may lead to variability in risk-taking among individuals when food is scarce or supply is unpredictable. This synergistic relationship between RMR and food deprivation could lead to an increased likelihood of being predated for individuals with a relatively high intrinsic energy demand during times when food is scarce.

The schooling behaviour of fish is of great biological importance, playing a crucial role in the foraging and predator avoidance of numerous species. The extent to which physiological performance traits affect the spatial positioning of individual fish within schools is completely unknown. Schools of juvenile mullet Liza aurata were filmed at three swim speeds in a swim tunnel, with one focal fish from each school then also measured for standard metabolic rate (SMR), maximal metabolic rate (MMR), aerobic scope (AS) and maximum aerobic swim speed. At faster speeds, fish with lower MMR and AS swam near the rear of schools. These trailing fish required fewer tail beats to swim at the same speed as individuals at the front of schools, indicating that posterior positions provide hydrodynamic benefits that reduce swimming costs. Conversely, fish with high aerobic capacity can withstand increased drag at the leading edge of schools, where they could maximize food intake while possibly retaining sufficient AS for other physiological functions. SMR was never related to position, suggesting that high maintenance costs do not necessarily motivate individuals to occupy frontal positions. In the wild, shifting of individuals to optimal spatial positions during changing conditions could influence structure or movement of entire schools.

For animals, being a member of a group provides various advantages, such as reduced vulnerability to predators, increased foraging opportunities and reduced energetic costs of locomotion. In moving groups such as fish schools, there are benefits of group membership for trailing individuals, who can reduce the cost of movement by exploiting the flow patterns generated by the individuals swimming ahead of them. However, whether positions relative to the closest neighbours (e.g. ahead, sided by side or behind) modulate the individual energetic cost of swimming is still unknown. Here, we addressed these questions in grey mullet Liza aurata by measuring tail-beat frequency and amplitude of 15 focal fish, swimming in separate schools, while swimming in isolation and in various positions relative to their closest neighbours, at three speeds. Our results demonstrate that, in a fish school, individuals in any position have reduced costs of swimming, compared to when they swim at the same speed but alone. Although fish swimming behind their neighbours save the most energy, even fish swimming ahead of their nearest neighbour were able to gain a net energetic benefit over swimming in isolation, including those swimming at the front of a school. Interestingly, this energetic saving was greatest at the lowest swimming speed measured in our study. Because any member of a school gains an energetic benefit compared to swimming alone, we suggest that the benefits of membership in moving groups may be more strongly linked to reducing the costs of locomotion than previously appreciated.

Summary 1.Inter-individual variation in metabolic rate exists in a wide range of taxa. While this variation appears to be linked to numerous aspects of animal behaviour and personality, the ecological relevance of these relationships is not understood. The behavioural response of individual fish to acute aquatic hypoxia, for example, could be related to metabolic rate via influences on oxygen demand or the willingness to take risks. Individuals with higher metabolic rates could show greater hypoxia-associated increases in activity that could allow them to locate areas with increased oxygen availability but that also make them susceptible to predation. Any relationship between metabolic rate and risk-taking behaviour among individual fish could therefore be modulated by environmental oxygen levels, perhaps becoming stronger as oxygen availability declines. 2. We measured spontaneous swimming activity as an index of risk-taking by juvenile European sea bass in normoxia, moderate hypoxia (40% air saturation) and severe hypoxia (20% air saturation) after being startled by a predator model. All fish were also separately measured for routine metabolic rate by measuring oxygen uptake. 3. In hypoxia, fish re-emerged from cover sooner after a simulated attack and were generally more active than when the same fish were startled in normoxia. In addition, individual activity and risk-taking in severe hypoxia were positively correlated with metabolic rate. Aquatic surface respiration was a major contributor towards increased activity in hypoxia and was positively related to metabolic rate during severe hypoxia. There were no relationships between risk-taking and metabolic rate in moderate hypoxia or normoxia. 4. Relative measures of risk-taking among individual fish were not consistent among oxygen levels, further suggesting that individuals differ in sensitivity to hypoxia and the degree to which this environmental stressor affects risk-taking behaviour. 5. These results suggest that fish with relatively high metabolic rates become more active during acute hypoxia, possibly leading to increased susceptibility to predation in response to differences in metabolic demand. In addition, the relationship between metabolic rate and risk-taking may only be observable during exposure to a physiological stressor or such a stressor may strengthen any relationships observable under more benign conditions.

Animals show consistent differences in behaviour and physiology. Understanding these differences is vital for predicting the effects of gradual environmental change, such as climate change and ocean acidification. Here we review how such trait repeatability is relevant for conservation of wild fish.

SUMMARYStudies of inter-individual variation in fish swimming performance may provide insight into how selection has influenced diversity in phenotypic traits. We investigated individual variation and short-term repeatability of individual swimming performance by wild European sea bass in a constant acceleration test (CAT). Fish were challenged with four consecutive CATs with 5min rest between trials. We measured maximum anaerobic speed at exhaustion (U CAT ), gait transition speed from steady aerobic to unsteady anaerobic swimming (U gt ), routine metabolic rate (RMR), post-CAT maximum metabolic rate (MMR), aerobic scope and recovery time from the CATs. Fish achieved significantly higher speeds during the first CAT (U CAT 170cms -1 ), and had much more inter-individual variation in performance (coefficient of variation, CV18.43%) than in the subsequent three tests (U CAT 134cms -1 ; CV7.3%), which were very repeatable among individuals. The individual variation in U CAT in the first trial could be accounted for almost exclusively by variation in anaerobic burst-and-coast performance beyond U gt . The U gt itself varied substantially between individuals (CV11.4%), but was significantly repeatable across all four trials. Individual RMR and MMR varied considerably, but the rank order of post-CAT MMR was highly repeatable. Recovery rate from the four CATs was highly variable and correlated positively with the first U CAT (longer recovery for higher speeds) but negatively with RMR and aerobic scope (shorter recovery for higher RMR and aerobic scope). This large variation in individual performance coupled with the strong correlations between some of the studied variables may reflect divergent selection favouring alternative strategies for foraging and avoiding predation.

The istiophorid family of billfishes is characterized by an extended rostrum or 'bill'. While various functions (e.g. foraging and hydrodynamic benefits) have been proposed for this structure, until now no study has directly investigated the mechanisms by which billfishes use their rostrum to feed on prey. Here, we present the first unequivocal evidence of how the bill is used by Atlantic sailfish (Istiophorus albicans) to attack schooling sardines in the open ocean. Using high-speed video-analysis, we show that (i) sailfish manage to insert their bill into sardine schools without eliciting an evasive response and (ii) subsequently use their bill to either tap on individual prey targets or to slash through the school with powerful lateral motions characterized by one of the highest accelerations ever recorded in an aquatic vertebrate. Our results demonstrate that the combination of stealth and rapid motion make the sailfish bill an extremely effective feeding adaptation for capturing schooling prey.