Stefano Marras

Environmental stressors alter relationships between physiology and behaviour.

Although correlations have frequently been observed between specific physiological and behavioural traits across a range of animal taxa, the nature of these associations has been shown to vary. Here we argue that a major source of this inconsistency is the influence of environmental stressors, which seem capable of revealing, masking, or modulating covariation in physiological and behavioural traits. These effects appear to be mediated by changes in the observed variation of traits and differential sensitivity to stressors among phenotypes. Considering that wild animals routinely face a range of biotic and abiotic stressors, increased knowledge of these effects is imperative for understanding the causal mechanisms of a range of ecological phenomena and evolutionary responses to stressors associated with environmental change.

Aerobic capacity influences the spatial position of individuals within fish schools

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.

Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass

1. 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.

Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax.

SUMMARY Studies 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 (UCAT), gait transition speed from steady aerobic to unsteady anaerobic swimming (Ugt), 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 (UCAT=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 (UCAT=134 cm s–1; CV=7.3%), which were very repeatable among individuals. The individual variation in UCAT in the first trial could be accounted for almost exclusively by variation in anaerobic burst-and-coast performance beyond Ugt. The Ugt 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 UCAT (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.

Fish swimming in schools save energy regardless of their spatial position.

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.

Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability

SUMMARY Inter-individual variation in physiological performance traits, which is stable over time, can be of potential ecological and evolutionary significance. The fish escape response is interesting in this regard because it is a performance trait for which inter-individual variation may determine individual survival. The temporal stability of such variation is, however, largely unexplored. We quantified individual variation of various components of the escape response in a population of European sea bass (Dicentrarchus labrax), considering both non-locomotor (responsiveness and latency) and locomotor (speed, acceleration, turning rate, turning angle and distance travelled in a fixed time, Desc) variables. We assessed whether variation in performance was temporally stable and we searched for any trade-offs among the components of the response that might explain why the variation persisted in the population. The coefficient of variation was high for all components, from 23% for turning rate to 41% for Desc, highlighting the non-stereotypic nature of the response. Individual performance for all variables was significantly repeatable over five sequential responses at 30 min intervals, and also repeatable after a 30 day interval for most of the components. This indicates that the variation is intrinsic to the individuals, but there was no evidence for trade-offs amongst the components of the response, suggesting that, if trade-offs exist, they must be against other ecologically important behavioural or performance traits.

Context dependency of trait repeatability and its relevance for management and conservation of fish populations

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.

Information transfer and antipredator maneuvers in schooling herring

Schooling behavior in fish has been recognized to confer antipredator advantages. However, the mechanisms that lead to various patterns of escape maneuvers in fish schools are largely unknown. Here, we investigated the effect of startle stimulus characteristics (distance and orientation) on the escape maneuvers of schools of a highly gregarious fish species, the Atlantic herring Clupea harengus. We quantified information transfer of the onset of startle responses by analyzing the speed of the waves of their propagation (Uw = 6.7 ± 1.6 m/s; mean ± SD). Uw was found to be positively correlated with the number of early responders (i.e., individuals reacting with a latency <50 ms). In addition, we identified the rules determining two different evading maneuvers: highly aligned maneuvers (i.e., all individuals oriented in a relatively uniform direction) and “split” maneuvers (i.e., individuals escaping with low directional uniformity). The pattern of escape maneuvers was dependent on stimulus direction (αs). Lateral stimulation (30° < αs < 120°) elicits highly aligned maneuvers away from the stimulus, while frontal stimulations (αs < 30°) causes split maneuvers, which are followed by realignment about 1 s after stimulation. These simple rules suggest that certain stimulus characteristics are important factors determining the variability of antipredator maneuvers observable in schooling fish.

Conservation physiology of marine fishes: advancing the predictive capacity of models

At the end of May, 17 scientists involved in an EU COST Action on Conservation Physiology of Marine Fishes met in Oristano, Sardinia, to discuss how physiology can be better used in modelling tools to aid in management of marine ecosystems. Current modelling approaches incorporate physiology to different extents, ranging from no explicit consideration to detailed physiological mechanisms, and across scales from a single fish to global fishery resources. Biologists from different sub-disciplines are collaborating to rise to the challenge of projecting future changes in distribution and productivity, assessing risks for local populations, or predicting and mitigating the spread of invasive species.

Predicting future thermal habitat suitability of competing native and invasive fish species: From metabolic scope to oceanographic modelling

Global increase in sea temperatures has been suggested to facilitate the incoming and spread of tropical invaders. Here, we determined the effect of temperature on the aerobic metabolic scope of two competing fish species, one native and one invasive, and we predicted their future thermal habitat suitability.