Guy Claireaux

Influence of temperature, oxygen and salinity on the metabolism of the European sea bass

Abstract Standard (SMR) and routine (RMR) metabolic rates of groups (4 to 5 individuals) of European sea bass (Dicentrarchus labrax) were measured at combinations of the following factors: temperature (10, 15, 20 and 25°C), oxygenation level (air saturation to 1.5 mg dm−3) and salinity (30, 20, 10 and 5‰). The influence of these environmental conditions on fish metabolic demand was then analysed through ANOVA. At 10, 15, 20 and 25°C, standard metabolic rates were 36, 65, 89, and 91 mg O2 kg−1 h−1, respectively, while routine oxygen consumptions covered most of the metabolic range accessible. Osmoregulatory costs are linked to metabolic activity through ventilation. This relationship was highlighted by the observed interaction between environmental salinity and temperature. We were, however, unable to detect interactions between salinity and routine metabolic rate, or between salinity and oxygenation level. In order to delineate more precisely the restrictions imposed by water oxygenation on fish metabolic performance we determined the limiting oxygen concentration curves at each experimental temperature. We followed up by modelling the bass active metabolic rate (AMR) and metabolic scope (MS) as functions of both ambient temperature and oxygenation. These mathematical models allowed the characterisation of the controlling and limiting effects of water temperature and oxygen content on the metabolic capacity of the species. Thus, AMR at 10, 15 and 20°C were estimated at 65, 160 and 360 mg O2 kg−1 h−1, respectively. However, at higher temperature (25°C) AMR dropped slightly (to 340 mg O2 kg−1 h−1). Bass MS increased by a factor of 9 between 10 and 20°C, but diminished at higher temperatures. The present study contributes to our current understanding of the influences of environmental factors on the metabolism of sea bass and provides a bioenergetic basis for a study of how environmental constraints govern the spatial and temporal distribution pattern of this species.

Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax).

SUMMARY This study is an attempt to gain an integrated understanding of the interactions between temperature, locomotion activity and metabolism in the European sea bass (Dicentrarchus labrax). To our knowledge this study is among the few that have investigated the influence of the seasonal changes in water temperature on swimming performance in fish. Using a Brett-type swim-tunnel respirometer the relationship between oxygen consumption and swimming speed was determined in fish acclimatised to 7, 11, 14, 18, 22, 26 and 30°C. The corresponding maximum swimming speed (Umax), optimal swimming speed (Uopt), active (AMR) and standard (SMR) metabolic rates as well as aerobic metabolic scope (MS) were calculated. Using simple mathematical functions, these parameters were modelled as a function of water temperature and swimming speed. Both SMR and AMR were positively related to water temperature up to 24°C. Above 24°C SMR and AMR levelled off and MS tended to decrease. We found a tight relationship between AMR and Umax and observed that raising the temperature increased AMR and increased swimming ability. However, although fish swam faster at high temperature, the net cost of transport (COTnet) at a given speed was not influence by the elevation of the water temperature. Although Uopt doubled between 7°C and 30°C (from 0.3 to 0.6 m s-1), metabolic rate at Uopt represented a relatively constant fraction of the animal active metabolic rate (40-45%). A proposed model integrates the effects of water temperature on the interaction between metabolism and swimming performance. In particular the controlling effect of temperature on AMR is shown to be the key factor limiting maximal swimming speed of sea bass.

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.

Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax)

SUMMARY The specific growth rate (SGR) of a cohort of 2000 tagged juvenile European sea bass was measured in a common tank, during two sequential cycles comprising three-weeks feed deprivation followed by three-weeks ad libitum re-feeding. After correction for initial size at age as fork length, there was a direct correlation between negative SGR (rate of mass loss) during feed deprivation and positive SGR (rate of compensatory growth) during re-feeding (Spearman rank correlation R=0.388, P=0.000002). Following a period of rearing under standard culture conditions, individuals representing ‘high growth’ phenotypes (GP) and ‘high tolerance of feed deprivation’ phenotypes (DP) were selected from either end of the SGR spectrum. Static and swimming respirometry could not demonstrate lower routine or standard metabolic rate in DP to account for greater tolerance of feed deprivation. Increased rates of compensatory growth in GP were not linked to greater maximum metabolic rate, aerobic metabolic scope or maximum cardiac performance than DP. When fed a standard ration, however, GP completed the specific dynamic action (SDA) response significantly faster than DP. Therefore, higher growth rate in GP was linked to greater capacity to process food. There was no difference in SDA coefficient, an indicator of energetic efficiency. The results indicate that individual variation in growth rate in sea bass reflects, in part, a trade-off against tolerance of food deprivation. The two phenotypes represented the opposing ends of a spectrum. The GP aims to exploit available resources and grow as rapidly as possible but at a cost of physiological and/or behavioural attributes, which lead to increased energy dissipation when food is not available. An opposing strategy, exemplified by DP, is less ‘boom and bust’, with a lower physiological capacity to exploit resources but which is less costly to sustain during periods of food deprivation.

Reflex cardioventilatory responses to hypoxia in the flathead gray mullet (Mugil cephalus) and their behavioral modulation by perceived threat of predation and water turbidity.

In hypoxia, gray mullet surface to ventilate well‐oxygenated water in contact with air, an adaptive response known as aquatic surface respiration (ASR). Reflex control of ASR and its behavioral modulation by perceived threat of aerial predation and turbid water were studied on mullet in a partly sheltered aquarium with free surface access. Injections of sodium cyanide (NaCN) into either the bloodstream (internal) or ventilatory water stream (external) revealed that ASR, hypoxic bradycardia, and branchial hyperventilation were stimulated by chemoreceptors sensitive to both systemic and water O2 levels. Sight of a model avian predator elicited bradycardia and hypoventilation, a fear response that inhibited reflex hyperventilation following external NaCN. The time lag to initiation of ASR following NaCN increased, but response intensity (number of events, time at the surface) was unchanged. Mullet, however, modified their behavior to surface under shelter or near the aquarium edges. Turbid water abolished the fear response and effects of the predator on gill ventilation and timing of ASR following external NaCN, presumably because of reduced visibility. However, in turbidity, mullet consistently performed ASR under shelter or near the aquarium edges. These adaptive modulations of ASR behavior would allow mullet to retain advantages of the chemoreflex when threatened by avian predators or when unable to perceive potential threats in turbidity.

Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar)

Improving fish robustness is of utmost relevance to reducing fish losses in farming. Although not previously examined, we hypothesized that aerobic training, as shown for human studies, could strengthen disease resistance in Atlantic salmon (Salmo salar). Thus, we exercised salmon pre-smolts for 6 weeks at two different aerobic training regimes; a continuous intensity training (CT; 0.8bls(-1)) and an interval training (IT; 0.8bl s(-1) 16h and 1.0bl s(-1) 8h) and compared them with untrained controls (C; 0.05bl s(-1)). The effects of endurance training on disease resistance were evaluated using an IPN virus challenge test, while the cardiac immune modulatory effects were characterized by qPCR and microarray gene expression analyses. In addition, swimming performance and growth parameters were investigated. Survival after the IPN challenge was higher for IT (74%) fish than for either CT (64%) or C (61%) fish. While both CT and IT groups showed lower cardiac transcription levels of TNF-α, IL-1β and IL-6 prior to the IPN challenge test, IT fish showed the strongest regulation of genes involved in immune responses and other processes known to affect disease resistance. Both CT and IT regimes resulted in better growth compared with control fish, with CT fish developing a better swimming efficiency during training. Overall, interval aerobic training improved growth and increased robustness of Atlantic salmon, manifested by better disease resistance, which we found was associated with a modulation of relevant gene classes on the cardiac transcriptome.

Gastrointestinal blood flow and postprandial metabolism in swimming sea bass Dicentrarchus labrax.

In trout and salmon, the metabolic costs of exercise and feeding are additive, which would suggest that gastrointestinal blood flow during exercise is maintained to preserve digestive and absorptive processes related to the specific dynamic action (SDA) of food. However, in most published studies, gastrointestinal blood flow drops during swimming, hypoxia, and general stress. To test whether gastrointestinal blood flow is spared during exercise after feeding, sea bass were instrumented with flow probes to measure cardiac output and celiacomesenteric blood flow while swimming in a respirometer before and after feeding. Swimming at 2 body lengths per second (bl s−1) increased metabolic rate considerably more than did feeding (208% vs. 32% increase, respectively, relative to resting), and a similar pattern was observed for cardiac output. In unfed fish, resting gastrointestinal blood flow was 13.8 ± 0.5 mL min−1 kg−1. After feeding, resting gastrointestinal blood flow increased by 82% but then decreased progressively with increasing swimming speeds. At 2 bl s−1, gastrointestinal blood flow in fed fish was not significantly different compared with that in unfed swimming fish, and, therefore, the data do not support the gastrointestinal sparing hypothesis. The magnitude of the SDA was maintained despite the decrease in gastrointestinal blood flow and the consequent reduction in oxygen supply to the gut. An estimate of maximal oxygen flow to the gastrointestinal tract after feeding yielded 2.6 mmol O2 h−1 kg−1, but this amount is not able to cover the oxygen demand of 3.16 mmol O2 h−1 kg−1. Therefore, the SDA must reflect metabolic processes in tissues other than those directly perfused by the celiacomesenteric artery.

Thermal and Temporal Stability of Swimming Performance in the European Sea Bass

Studies of locomotor performance have contributed to the elucidation of how suborganismal traits ultimately relate to fitness. In terrestrial populations, exploring the physiological and environmental contributions to whole‐animal performance measures has improved our understanding of phenotypic selection. Conversely, very little is known about the links between phenotypic selection and swimming abilities in fish. Most research on swimming performance in fish has focused on morphological, physiological, and biochemical traits contributing to performance or has used swimming performance as a measure of environmental suitability. Few studies have explored how swimming performance is integrated with life‐history traits or contributes to Darwinian fitness. In addition, while there are many studies on how the environment influences the swimming performance of fish, few have been done at the individual level. The objective of this study was to broaden our understanding of the relevance of fish swimming performance studies by testing the hypothesis that swimming performance (endurance and sprint) is ontogenetically and temporally stable across fluctuating environmental conditions. We found that individual sprint performances recorded at 12°C were significantly repeatable after a 4‐wk acclimation to 22°C, although relative sprint performance of fish that survived 6 mo of natural conditions in a mesocosm was not significantly repeatable. Endurance swimming performance, as measured by critical swimming speed (Ucrit) before and after the 6‐mo exposure to simulated natural conditions, was significantly repeatable within survivors. Relative sprint and critical swimming performances were not significantly related to each other. We concluded that within a time frame of up to 6 mo, the swimming performances of individual bass are ontogenetically nearly stable (sprint) to stable (endurance) despite large fluctuations in environmental conditions. Moreover, because they rely on different physiological performance traits, critical swimming and sprinting follow different patterns of change. This observation suggests the absence of a trade‐off between these two swimming modes and introduces the possibly of independent selection trajectories.

Associations between tissue fatty acid composition and physiological traits of performance and metabolism in the seabass (Dicentrarchus labrax)

SUMMARY Seabass were fed for 4 months with diets where the lipid was provided as either canola oil (CO), palm oil (PO) or fish oil (FO), to generate diversity in their tissue fatty acid (FA) composition and investigate how this influenced major traits of exercise performance, cardiac performance and respiratory metabolism. In particular, based upon previous observations, we investigated the hypothesis that enriching the fish tissues with oleic and linoleic acids (OA, 18:1n-9 and LA, 18:2n-6, respectively) from the CO and PO diets would improve maximum exercise and cardiac performance, and increase aerobic metabolic scope. This proved to be the case; exercise respirometry on bass fitted with cardiac flow probes revealed that those fed CO and PO diets had a significantly higher critical swimming speed (Ucrit) than those fed the FO diet. The improved swimming performance in the CO and PO groups was accompanied by a higher maximum cardiac output (Q̇) and net cardiac scope, and a higher active metabolic rate (AMR) and aerobic scope (AS) than in the FO group. Analysis of tissue FA composition revealed that the fish fed the CO and PO diets had accumulated significantly higher levels of OA and LA in their heart and muscle than the fish from the FO group, which had significantly higher levels of highly unsaturated FA of the n-3 series, such as EPA and DHA (20:5n-3 and 22:6n-3, respectively). Principal components analysis revealed significant positive associations between tissue OA and LA content and Ucrit, maximum Q, the increase in Q during exercise, AMR and aerobic scope. There was a negative association between these physiological traits and tissue content of EPA. Therefore, diet composition is an environmental factor that can generate significant phenotypic diversity in major physiological traits of performance and metabolism in the seabass, with increased intake of FAs such as OA and LA leading to improved cardiorespiratory performance.

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.