Towards the integration of ecophysiology with fisheries stock assessment for conservation policy and evaluating the status of the Mediterranean Sea.

Recent European Union (EU) regulations have been introduced to discourage the capture of undersized specimens with the aim of reducing the bycatch mortality imposed by commercial fisheries. We argue that we still lack accurate data regarding basic information required to properly implement these regulations for most Mediterranean ecosystems, including the true mortality imposed by fisheries, escape rates from fishing gears and the capability of specimens to survive following discard. We suggest that additional reliance on physiological biomarkers could assist in all aspects of the data collection required to support implementation of the EU discard ban (aka landing obligation), particularly in determining which species should receive special dispensation from this policy. Ideally, this new approach, here termed the 'Fisheries Environmental and Physiological Stress Analysis' (FEPSA), would become an important step for any fish stock assessment within the ecosystem approach to fisheries management and the recognition of Good Environmental Status, as established by the EU in the Marine Strategy Framework Directive (2008/56/EC). In particular, the main goal of FEPSA would be applying the study of physiological stressors to exploited stocks to estimate the so-called collateral fishing mortality, which includes the mortality experienced by fish that escape after interacting with fishing gears or that are discarded, with some degree of injury or physiological stress. The approach outlined here, which is described for bottom trawls but adaptable to any other type of fishing gear, is not a trivial undertaking but is a requirement for collecting the data required by recent EU fisheries policies. While we agree that the threats to marine biodiversity posed by fishing and associated discard practices require strong policy interventions, we emphasize that the research programs needed to support such initiatives, including the landing obligation, should be given equal priority. This is particularly true for Mediterranean fisheries, which are at a complex intersection of jurisdictional boundaries, numerous additional ecosystem threats including widespread pollution, thermal variation and hypoxia, and are historically understudied as compared to fisheries and species in more northern climates.

Intraspecific variation in thermal tolerance differs between tropical and temperate fishes.

How ectothermic animals will cope with global warming is a critical determinant of the ecological impacts of climate change. There has been extensive study of upper thermal tolerance limits among fish species but how intraspecific variation in tolerance may be affected by habitat characteristics and evolutionary history has not been considered. Intraspecific variation is a primary determinant of species vulnerability to climate change, with implications for global patterns of impacts of ongoing warming. Using published critical thermal maximum (CTmax) data on 203 fish species, we found that intraspecific variation in upper thermal tolerance varies according to a species' latitude and evolutionary history. Overall, tropical species show a lower intraspecific variation in thermal tolerance than temperate species. Notably, freshwater tropical species have a lower variation in tolerance than freshwater temperate species, which implies increased vulnerability to impacts of thermal stress. The extent of variation in CTmax among fish species has a strong phylogenetic signal, which may indicate a constraint on evolvability to rising temperatures in tropical fishes. That is, in addition to living closer to their upper thermal limits, tropical species may have higher sensitivity and lower adaptability to global warming compared to temperate counterparts. This is evidence that freshwater tropical fish communities, worldwide, are especially vulnerable to ongoing climate change.

Shoal familiarity modulates effects of individual metabolism on vulnerability to capture by trawling.

Impacts of fisheries-induced evolution may extend beyond life history traits to more cryptic aspects of biology, such as behaviour and physiology. Understanding roles of physiological traits in determining individual susceptibility to capture in fishing gears and how these mechanisms change across contexts is essential to evaluate the capacity of commercial fisheries to elicit phenotypic change in exploited populations. Previous work has shown that metabolic traits related to anaerobic swimming may determine individual susceptibility to capture in trawls, with fish exhibiting higher anaerobic performance more likely to evade capture. However, high densities of fish aggregated ahead of a trawl net may exacerbate the role of social interactions in determining an individual fish's behaviour and likelihood of capture, yet the role of social environment in modulating relationships between individual physiological traits and vulnerability to capture in trawls remains unknown. By replicating the final moments of capture in a trawl using shoals of wild minnow (Phoxinus phoxinus), we investigated the role of individual metabolic traits in determining susceptibility to capture among shoals of both familiar and unfamiliar conspecifics. We expected that increased shoal cohesion and conformity of behaviour in shoals of familiar fish would lessen the role of individual metabolic traits in determining susceptibility to capture. However, the opposite pattern was observed, with individual fish exhibiting high anaerobic capacity less vulnerable to capture in the trawl net, but only when tested alongside familiar conspecifics. This pattern is likely due to stronger cohesion within familiar shoals, where maintaining a minimal distance from conspecifics, and thus staying ahead of the net, becomes limited by individual anaerobic swim performance. In contrast, lower shoal cohesion and synchronicity of behaviours within unfamiliar shoals may exacerbate the role of stochastic processes in determining susceptibility to capture, disrupting relationships between individual metabolic traits and vulnerability to capture.

Individual variation in the compromise between social group membership and exposure to preferred temperatures.

Group living is widespread among animal species, and comes with a number of costs and benefits associated with foraging, predator avoidance and reproduction. It is largely unknown, however, whether individuals sacrifice exposure to their own preferred or optimal environmental conditions so they can remain part of a social group. Here, we demonstrate that individual three-spine sticklebacks vary in the degree to which they forego exposure to their preferred ambient temperature so they can associate with a group of conspecifics. Individual fish varied widely in preferred temperature when tested in isolation. When the same individuals were presented with a choice of a warm or cold thermal regime in the presence of a social group in one of the environments, fish spent more time with the group if it was close to their own individually preferred temperature. When a group was in a relatively cool environment, focal individuals that were more social deviated most strongly from their preferred temperature to associate with the group. Standard and maximum metabolic rate were not related to temperature preference or thermal compromise. However, individuals with a higher standard metabolic rate were less social, and so energetic demand may indirectly influence the environmental costs experienced by group members. The reduced tendency to engage with a social group when there is a large difference between the group temperature and the individual's preferred temperature suggests a role for temperature in group formation and cohesion that is mediated by individual physiology and behaviour. Together, these data highlight exposure to non-preferred temperatures as a potential cost of group membership that probably has important but to date unrecognized implications for metabolic demand, energy allocation, locomotor performance and overall group functioning.

Do method and species lifestyle affect measures of maximum metabolic rate in fishes?

The rate at which active animals can expend energy is limited by their maximum aerobic metabolic rate (MMR). Two methods are commonly used to estimate MMR as oxygen uptake in fishes, namely during prolonged swimming or immediately following brief exhaustive exercise, but it is unclear whether they return different estimates of MMR or whether their effectiveness for estimating MMR varies among species with different lifestyles. A broad comparative analysis of MMR data from 121 fish species revealed little evidence of different results between the two methods, either for fishes in general or for species of benthic, benthopelagic or pelagic lifestyles.

Body length rather than routine metabolic rate and body condition correlates with activity and risk-taking in juvenile zebrafish Danio rerio.

In this study, the following hypotheses were explored using zebrafish Danio rerio: (1) individuals from the same cohort differ consistently in activity and risk-taking and (2) variation in activity and risk-taking is linked to individual differences in metabolic rate, body length and body condition. To examine these hypotheses, juvenile D. rerio were tested for routine metabolic rate and subsequently exposed to an open field test. Strong evidence was found for consistent among-individual differences in activity and risk-taking, which were overall negatively correlated with body length, i.e. larger D. rerio were found to be less active in a potentially dangerous open field and a similar trend was found with respect to a more direct measure of their risk-taking tendency. In contrast, routine metabolic rate and body condition were uncorrelated with both activity and risk-taking of juvenile D. rerio. These findings suggest that body length is associated with risk-related behaviours in juvenile D. rerio for which larger, rather than smaller, individuals may have a higher risk of predation, while the role for routine metabolic rate is relatively limited or non-existent, at least under the conditions of the present study.

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

Repeatability of behavioural and physiological traits is increasingly a focus for animal researchers, for which fish have become important models. Almost all of this work has been done in the context of evolutionary ecology, with few explicit attempts to apply repeatability and context dependency of trait variation toward understanding conservation-related issues. Here, we review work examining the degree to which repeatability of traits (such as boldness, swimming performance, metabolic rate and stress responsiveness) is context dependent. We review methods for quantifying repeatability (distinguishing between within-context and across-context repeatability) and confounding factors that may be especially problematic when attempting to measure repeatability in wild fish. Environmental factors such temperature, food availability, oxygen availability, hypercapnia, flow regime and pollutants all appear to alter trait repeatability in fishes. This suggests that anthropogenic environmental change could alter evolutionary trajectories by changing which individuals achieve the greatest fitness in a given set of conditions. Gaining a greater understanding of these effects will be crucial for our ability to forecast the effects of gradual environmental change, such as climate change and ocean acidification, the study of which is currently limited by our ability to examine trait changes over relatively short time scales. Also discussed are situations in which recent advances in technologies associated with electronic tags (biotelemetry and biologging) and respirometry will help to facilitate increased quantification of repeatability for physiological and integrative traits, which so far lag behind measures of repeatability of behavioural traits.

Does individual variation in metabolic phenotype predict fish behaviour and performance?

There is increasing interest in documenting and explaining the existence of marked intraspecific variation in metabolic rate in animals, with fishes providing some of the best-studied examples. After accounting for variation due to other factors, there can typically be a two to three-fold variation among individual fishes for both standard and maximum metabolic rate (SMR and MMR). This variation is reasonably consistent over time (provided that conditions remain stable), and its underlying causes may be influenced by both genes and developmental conditions. In this paper, current knowledge of the extent and causes of individual variation in SMR, MMR and aerobic scope (AS), collectively its metabolic phenotype, is reviewed and potential links among metabolism, behaviour and performance are described. Intraspecific variation in metabolism has been found to be related to other traits: fishes with a relatively high SMR tend to be more dominant and grow faster in high food environments, but may lose their advantage and are more prone to risk-taking when conditions deteriorate. In contrast to the wide body of research examining links between SMR and behavioural traits, very little work has been directed towards understanding the ecological consequences of individual variation in MMR and AS. Although AS can differ among populations of the same species in response to performance demands, virtually nothing is known about the effects of AS on individual behaviours such as those associated with foraging or predator avoidance. Further, while factors such as food availability, temperature, hypoxia and the fish's social environment are known to alter resting and MMRs in fishes, there is a paucity of studies examining how these effects vary among individuals, and how this variation relates to behaviour. Given the observed links between metabolism and measures of performance, understanding the metabolic responses of individuals to changing environments will be a key area for future research because the environment will have a strong influence on which animals survive predation, become dominant and ultimately have the highest reproductive success. Although current evidence suggests that variation in SMR may be maintained within populations via context-dependent fitness benefits, it is suggested that a more integrative approach is now required to fully understand how the environment can modulate individual performance via effects on metabolic phenotypes encompassing SMR, MMR and AS.

What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because self-maintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the 'maintenance costs' of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.

Sub-lethal ammonia toxicity in largemouth bass.

Guidelines for ammonia toxicity in fish are often determined using static exposure tests with immature fish over a 96-h period. These results may not be relevant to aquaculture, hauling or angling tournament scenarios where mature fish can be exposed to ammonia for shorter durations, often following additional stressors such as handling. The current study sought to quantify (1) the impact of ambient ammonia on the ability of largemouth bass to recover from exercise, (2) the behavioural response of largemouth bass to elevated ambient ammonia and (3) the concentration of ammonia that can accumulate in a live-release vessel at an angling tournament. After approximately 3 h, total ammonia (T(amm)) concentrations in a live-release vessel at an angling tournament were almost 200 muM. Exposure of fish to 1000 microM T(amm) (a value approximately 80% below the criteria maximum concentration for largemouth bass) caused significant reductions in ventilation rates, and increases in erratic swimming and irregular ventilation. Exposure to 100 microM T(amm) impaired the ability of largemouth bass to recover from exercise relative to fish recovering in fresh water. Therefore, sub-lethal ambient ammonia concentrations cause physiological disturbances that can impair the recovery of largemouth bass from exercise.