Article

Maxed Out: Optimizing Accuracy, Precision, and Power for Field Measures of Maximum Metabolic Rate in Fishes

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Abstract

Both laboratory and field respirometry are rapidly growing techniques to determine animal performance thresholds. However, replicating protocols to estimate maximum metabolic rate (MMR) between species, populations, and individuals can be difficult, especially in the field. We therefore evaluated seven different exercise treatments-four laboratory methods involving a swim tunnel (critical swim speed [Ucrit], Ucrit postswim fatigue, maximum swim speed [Umax], and Umax postswim fatigue) and three field-based chasing methods (3-min chase with 1-min air exposure, 3-min chase with no air exposure, and chase to exhaustion)-in adult coho salmon (Oncorhynchus kisutch) as a case study to determine best general practices for measuring and quantifying MMR in fish. We found that all seven methods were highly comparable and that chase treatments represent a valuable field alternative to swim tunnels. Moreover, we caution that the type of test and duration of measurement windows used to calculate MMR can have significant effects on estimates of MMR and statistical power for each approach.

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... Fish were introduced to a 'chase tank' (diameter, 1.8 m; 2000 L, filled to ∼660 L), where 4 people manually motivated the fish to burst swim continuously without allowing time for recovery, simulating predator evasion (Donaldson et al., 2010) or 'catch and release' fisheries interactions by making quick movements with their hands under the water, often lightly touching the fish's caudal fin. Chases occurred between 11:30 and 13:00 and lasted for 3 min, followed by 1-min air exposure, before fish were placed into a respirometer (Robinson et al., 2013;Little et al., 2020a). Dissolved oxygen recordings were initiated as soon as the respirometer lid was sealed and the chamber was flushed of all air bubbles (within 50-120 s post-chase). ...
... However, migratory salmon are reproductively active and so we applied the term RMR to the average of the lowest 10% of MO 2 values measured over ∼20 h recovery period and used this to calculate AAS (Chabot et al., 2016;Rosewarne et al., 2016). MMR was calculated from the slope during the steepest 60 s from the first measurement period (Norin and Clark, 2016;Little et al., 2020a). However, if the metabolic rate was higher at any point during the recovery phase, the MO 2 value of that entire measurement cycle was used to represent MMR instead (14 of 56 fish). ...
... MMR swim was measured as the steepest decline in dissolved oxygen recorded over any 3-min measurement period within either of the last two U crit test increments (Little et al., 2020a). MMR recovery was calculated from the first 10 min of recovery data (i.e. ...
Article
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Adult female Pacific salmon can have higher migration mortality rates than males, particularly at warm temperatures. However, the mechanisms underlying this phenomenon remain a mystery. Given the importance of swimming energetics on fitness, we measured critical swim speed, swimming metabolism, cost of transport, aerobic scope (absolute and factorial) and exercise recovery in adult female and male coho salmon (Oncorhynchus kisutch) held for 2 days at 3 environmentally relevant temperatures (9°C, 14°C, 18°C) in fresh water. Critical swimming performance (Ucrit) was equivalent between sexes and maximal at 14°C. Absolute aerobic scope was sex- and temperature-independent, whereas factorial aerobic scope decreased with increasing temperature in both sexes. The full cost of recovery from exhaustive exercise (excess post-exercise oxygen consumption) was higher in males compared to females. Immediately following exhaustive exercise (i.e. 1 h), recovery was impaired at 18°C for both sexes. At an intermediate time scale (i.e. 5 h), recovery in males was compromised at 14°C and 18°C compared to females. Overall, swimming, aerobic metabolism, and recovery energetics do not appear to explain the phenomenon of increased mortality rates in female coho salmon. However, our results suggest that warming temperatures compromise recovery following exhaustive exercise in both male and female salmon, which may delay migration progression and could contribute to en route mortality.
... 10-20-min-long background measurement (without a fish) for static respirometers (matching to the exact chamber) and ca. 20 ...
... An analysis of data extracted from the literature suggested that MMR is not sensitive to methodology, but that analysis did not focus on experiments specifically designed to address methodology (Killen et al. 2017). In contrast to our results, Little et al. (2020) did not detect differences among methods, including those we used here, in mature coho salmon (Oncorhynchus kisutch) at a single temperature (9 • C). In other cases, researchers who have set out to look for differences in MMR between swim tunnel respirometry and the chase method have typically found them. ...
... our study where fish were in a static respirometer). Likewise, Little et al. (2020) foundṀ O2 to be markedly lower during recovery from U max or U crit swimming even while fish received gentle ram ventilation in a swim tunnel. These findings from the literature might appear to invalidate our hypothesis about ram ventilation being responsible for fish reaching higheṙ M O2 in a swim tunnel respirometer (cf. ...
Article
Experimental biologists now routinely quantify maximum metabolic rate (MMR) in fishes using respirometry, often with the goal of calculating aerobic scope and answering important ecological and evolutionary questions. Methods used for estimating MMR vary considerably, with the two most common methods being (i) the ‘chase method’, where fish are manually chased to exhaustion and immediately sealed into a respirometer for post-exercise measurement of oxygen consumption rate (ṀO2), and (ii) the ‘swim tunnel method’, whereby ṀO2 is measured while the fish swims at high speed in a swim tunnel respirometer. In this study, we compared estimates for MMR made using a 3-min exhaustive chase (followed by measurement of ṀO2 in a static respirometer) versus those made via maximal swimming in a swim tunnel respirometer. We made a total of 134 estimates of MMR using the two methods with juveniles of two salmonids (Atlantic salmon Salmo salar and Chinook salmon Oncorhynchus tshawytscha) across a 6°C temperature range. We found that the chase method underestimated ‘true’ MMR (based on the swim tunnel method) by ca. 20% in these species. The gap in MMR estimates between the two methods was not significantly affected by temperature (range of ca. 15–21°C) nor was it affected by body mass (overall range of 53.5–236 g). Our data support some previous studies that have suggested the use of a swim tunnel respirometer generates markedly higher estimates of MMR than does the chase method, at least for species in which a swim tunnel respirometer is viable (e.g. ‘athletic’ ram ventilating fishes). We recommend that the chase method could be used as a ‘proxy’ (i.e. with a correction factor) for MMR in future studies if supported by a species-specific calibration with a relevant range of temperatures, body sizes or other covariates of interest.
... Individual fish were manually chased by hand for 3 min to exhaustion in a large cooler (45.4 L). This is a standard protocol that has been frequently used to exhaust fish (Norin and Clark, 2016;Little et al., 2020). The fish were then air-exposed for 30 s before being immediately placed in a respirometry chamber at which time measurement of oxygen consumption began and continued for 18-24 h (Eliason et al., 2008) (Fig. 2). ...
... The corresponding temperature values for each MO 2 measurement used in the SMR calculation were averaged to determine the mean temperature for SMR for each fish. Maximum metabolic rate (MMR; mg O 2 kg −1 min −1 ), the upper boundary for aerobic metabolism that is achievable by an animal, was measured immediately after the 3-min chase and 30-s air exposure once fish were placed in the respirometry chambers (Little et al., 2020). For the ambient trial, the temperature at which MMR was measured did not match the SMR temperature because SMR was measured over a range of temperatures during the diurnal cycle. ...
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Fish physiological performance is directly regulated by their thermal environment. Intraspecific comparisons are essential to ascertain the vulnerability of fish populations to climate change and to identify which populations may be more susceptible to extirpation and which may be more resilient to continued warming. In this study, we sought to evaluate how thermal performance varies in coastal cutthroat trout (Oncorhynchus clarki clarki) across four distinct watersheds in OR, USA. Specifically, we measured oxygen consumption rates in trout from the four watersheds with variable hydrologic and thermal regimes, comparing three ecologically relevant temperature treatments (ambient, annual maximum and novel warm). Coastal cutthroat trout displayed considerable intraspecific variability in physiological performance and thermal tolerance across the four watersheds. Thermal tolerance matched the historical experience: the coastal watersheds experiencing warmer ambient temperatures had higher critical thermal tolerance compared with the interior, cooler Willamette watersheds. Physiological performance varied across all four watersheds and there was evidence of a trade-off between high aerobic performance and broad thermal tolerance. Given the evidence of climate regime shifts across the globe, the uncertainty in both the rate and extent of warming and species responses in the near and long term, a more nuanced approach to the management and conservation of native fish species must be considered.
... basin (Diameter: 90 cm, Height: 30 cm) on the boat containing ~115 L lake water. The fish were subsequently subjected to a chase protocol for 3 min to elicit maximum heart rate, during which the fish was encouraged to swim by carefully prodding the caudal peduncle and fin (see Little et al., 2020;Prystay et al., 2019). The fish were then placed in a cooler (66 * 34 * 31 cm, 70 L) containing lake water for one hour of postchase maximum heart rate recordings, during which the water was partially exchanged several times to replenish water oxygen levels, remove deleterious metabolic by-products and to maintain a stable water temperature. ...
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The capacity to extract oxygen from the water, and the ability of the heart to drive tissue oxygen transport, are fundamental determinants of important life-history performance traits in fish. Cardiac performance is in turn dependent on the heart's own oxygen supply, which in some teleost species is partly delivered via a coronary circulation originating directly from the gills that perfuses the heart, and is crucial for cardiac, metabolic and locomotory capacities. It is currently unknown, however, how a compromised branchial blood flow (e.g., by angling-induced hook damage to the gills), constraining oxygen uptake and coronary blood flow, affects the energetically demanding parental care behaviours and reproductive fitness in fish. Here, we tested the hypothesis that blocking ¼ of the branchial blood flow and abolishing coronary blood flow would negatively affect parental care behaviours, cardiac performance (heart rate metrics, via implanted Star-Oddi heart rate loggers) and reproductive fitness of paternal smallmouth bass (Micropterus dolomieu). Our findings reveal that branchial/coronary ligation compromised reproductive fitness, as reflected by a lower proportion of broods reaching free-swimming fry and a tendency for a higher nest abandonment rate relative to sham operated control fish. While this was associated with a tendency for a reduced aggression in ligated fish, parental care behaviours were largely unaffected by the ligation. Moreover, the ligation did not impair any of the heart rate performance metrics. Our findings highlight that gill damage may compromise reproductive output of smallmouth bass populations during the spawning season. Yet, the mechanism(s) behind this finding remains elusive.
... We used two methods to identify the slope of the steepest decrease in O 2 saturation. First, we used respR [62] with the function auto_rate, fitting 1 min and 2 min windows [63] (example slope in electronic supplementary material, figure S5A). Second, slopes for MMR were extracted using a derivative of a polynomial curve fitted on each measurement (function smooth.spline, ...
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A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions (vgll3 and six6) makes Atlantic salmon (Salmo salar) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes-standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS)-and the life-history genomic regions, and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Furthermore, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve.
... SMR was calculated as the lowest 15% quantile of all recorded measurement cycles (Chabot et al., 2016). MMR was calculated as the steepest 120 s slope during the first measurement period (Little et al., 2020b; N=6-11 per treatment). All presented metabolic rate measurements are body mass specific (i.e. ...
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Thermal acclimation is a key process enabling ectotherms to cope with temperature change. To undergo a successful acclimation response, ectotherms require energy and nutritional building blocks obtained from their diet. However, diet is often overlooked as a factor that can alter acclimation responses. Using a temperate omnivorous fish, opaleye (Girella nigricans), as a model system, we tested the hypotheses that 1) diet can impact the magnitude of thermal acclimation responses and 2) traits vary in their sensitivity to both temperature acclimation and diet. We fed opaleye a simple omnivorous diet (ad libitum Artemia sp. and Ulva sp.) or a carnivorous diet (ad libitum Artemia sp.) at two ecologically relevant temperatures (12 and 20°C) and measured a suite of whole animal (growth, sprint speed, metabolism), organ (cardiac thermal tolerance), and cellular-level traits (oxidative stress, glycolytic capacity). When opaleye were offered two diet options compared to one, they had reduced cardiovascular thermal performance and higher standard metabolic rate under conditions representative of the maximal seasonal temperature the population experiences (20°C). Further, sprint speed and absolute aerobic scope were insensitive to diet and temperature, while growth was highly sensitive to temperature but not diet, and standard metabolic rate and maximum heart rate were sensitive to both diet and temperature. Our results reveal that diet influences thermal performance in trait-specific ways, which could create diet trade-offs for generalist ectotherms living in thermally variable environments. Ectotherms that alter their diet may be able to regulate their performance at different environmental temperatures.
... The standardization of experimental approaches for estimating MMR is improving as a growing number of studies outline the design and setup of associated respirometry experiments (Cech Jr. & Brauner, 2011;Chabot et al., 2016;Clark et al., 2013;Nelson, 2016;. However, the analytical process of actually estimating MMR from the experimental oxygen consumption data immediately following exhaustive exercise or air exposure-specifically, the statistical algorithm used to regress oxygen consumption over time-has not been systematically tested or standardized, despite recent recognition that these analytical choices affect MMR estimates (Little et al., 2020;Zhang et al., 2019Zhang et al., , 2020. Often, details concerning the analytical approach used to estimate MMR are not clearly reported, and when provided, there is usually little or no explanation as to why those specific methods were chosen. ...
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Advances in experimental design and equipment have simplified the collection of maximum metabolic rate (MMR) data for a more diverse array of water-breathing animals. However, little attention has been given to the consequences of analytical choices in the estimation of MMR. Using different analytical methods can reduce the comparability of MMR estimates across species and studies and has consequences for the burgeoning number of macroecological meta-analyses using metabolic rate data. Two key analytical choices that require standardization are the time interval, or regression window width, over which MMR is estimated, and the method used to locate that regression window within the raw oxygen depletion trace. Here, we consider the effect of both choices by estimating MMR for two shark and two salmo- nid species of different activity levels using multiple regression window widths and three analytical methods: rolling regression, sequential regression, and segmented regression. Shorter regression windows yielded higher metabolic rate estimates, with a risk that the shortest windows (<1-min) reflect more system noise than MMR signal. Rolling regression was the best candidate model and produced the highest MMR estimates. Sequential regression models consistently produced lower relative esti- mates than rolling regression models, while the segmented regression model was un- able to produce consistent MMR estimates across individuals. The time-point of the MMR regression window along the oxygen consumption trace varied considerably across individuals but not across models. We show that choice of analytical method, in addition to more widely understood experimental choices, profoundly affect the resultant estimates of MMR. We recommend that researchers (1) employ a rolling regression model with a reliable regression window tailored to their experimental system and (2) explicitly report their analytical methods, including publishing raw data and code.
... There is some evidence that standardized chase protocols used to estimate MMR may underestimate the true MMR value that would be obtained by using other protocols (i.e., swim tunnel respirometer) and that the shape of the AS curve could be biased by the use of a suboptimal method for estimating MMR (Hvas and Oppedal 2019;Raby et al. 2020). However, Mochnacz et al. (2017) and Little et al. (2020) have separately shown that for salmonids, a nonstandardized chase protocol, such as the one used in this study, is equal to estimating MMR with swim tunnel testing. MMR measured here is the ability of the fish to consume oxygen while recovering from anaerobic swimming; thus, a high MMR might indicate a fish's ability to undertake processes such as digestion simultaneously with activities like swimming. ...
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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.
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How phenotypic plasticity of locomotor performance varies among populations in nature is poorly known. Swimming ability of blacknose dace (Rhinichthys atratulus) from eight different watersheds had previously been shown to depend upon watershed impervious surface cover (ISC) and stream base-flow. Keeping these populations of stream fish under low flow conditions produced changes in locomotor capacity suggestive of phenotypic plasticity varying among the populations. The present experiments were conducted to better understand the plasticity of swimming performance in dace and how urbanization affects dace biology. Two experimental approaches were used: 1) laboratory training of dace populations at two levels of flow for 6 weeks; and, 2) exploring in situ training by capturing fish from relatively fast and slow reaches of three different streams and comparing their swimming abilities at three different scales. Individual sprint and endurance (modified Ucrit) swimming were significantly repeatable across a laboratory training regimen; sprint performance had previously been shown to not be repeatable when dace were held in static water. Both of our approaches suggested that sprint and endurance swimming ability significantly respond to changes in environmental flow. Although there was no evidence for a different magnitude of phenotypic plasticity among populations, urban populations that experience more stochastic flow regimes had more consistent plasticity. Phenotypic plasticity of locomotor performance in response to variable flow appears to be an important characteristic of blacknose dace biology, yet we did not uncover sufficient evidence to suggest that it is under selection in fish adjusting to urban stream habitats.
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We assessed the prolonged swimming performance (Ucrit), metabolic rate (ṀO2-min and ṀO2-max), and oxygen cost of transport (COT) for upper Fraser River pink salmon (Oncorhynchus gorbuscha (Walbaum, 1792); 53.5 ± 0.7 cm FL) and sockeye salmon (Oncorhynchus nerka (Walbaum, 1792); 59.3 ± 0.8 cm FL) across a range of naturally occurring river temperatures using large Brett-type swim tunnel respirometers. Pink salmon were capable of similar relative critical swimming speeds (Ucrit) as sockeye salmon (2.25 FL·s-1), but sockeye salmon swam to a higher absolute Ucrit (125.9 cm·s-1) than pink salmon (116.4 cm·s-1) because of their larger size. Nevertheless, three individual pink salmon (Ucrit-max = 173.6 cm·s-1) swam faster than any sockeye salmon (Ucrit-max = 157.0 cm·s-1), indicating that pink salmon are far better swimmers than has been previously assumed. Metabolic rate increased exponentially with swimming speed in both species and was highest for pink salmon, but swimming efficiency (i.e., COT) did not differ between species at their optimal swimming speeds. The upper and lower limits of metabolism did not differ between species and both ṀO2-min and ṀO2-max increased exponentially with temperature, but aerobic costs of transport were independent of temperature in both species. Strong thermal dependence of both swimming performance and COT were expected but not demonstrated in either species. Overall, a higher degree of inter-individual variability in pink salmon swim performance and capacity suggests that this species might not be as locally adapted to particular river migration conditions as are sockeye salmon.
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Under certain conditions, a number of fish species may perform brief excursions into severe hypoxia and return to water with a higher oxygen content. The term severe hypoxia describes oxygen conditions that are below the critical oxygen saturation (S(crit)), defined here as the oxygen threshold at which the standard metabolic rate becomes dependent upon the ambient oxygen content. Using rainbow trout (Oncorhynchus mykiss (Walbaum, 1792), this study quantified the excess posthypoxic oxygen consumption (EPHOC) occurring after exposure to oxygen availability below S(crit). Tests showed that S(crit) was 13.5% air saturation (O(2sat)). Fish were exposed to 10% O(2sat) for 0.97 h, and the EPHOC was quantified in normoxia (>= 95% O(2sat)) and hypoxia (30% O(2sat)) to test the hypothesis that reduced oxygen availability would decrease the peak metabolic rate (MO(2peak)) and prolong the duration of the metabolic recovery. Results showed that MO(2peak) during the recovery was reduced from 253 to 127 mg O(2).kg(-1).h(-1) in hypoxia compared with normoxia. Metabolic recovery lasted 5.2 h in normoxia and 9.8 h in hypoxia. The EPHOC, however, did not differ between the two treatments. Impeded metabolic recovery in hypoxia may have implications for fish recovering from exposure to oxygen availability below S(crit).
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Juvenile cod (Gadus morhua) were made to swim in a tunnel respirometer to determine the oxygen consumption during swimming at different speeds. Results were compared with measurements of standard and active metabolic rates in static respirometers before and after intense exercise. The oxygen consumption at maximum sustainable swimming speed was considerably lower than the peak oxygen consumption following exhausting exercise. It is suggested that these fish have a poorly developed system of aerobic (red) locomotor muscles which do not normally make a major demand upon oxygen consumption. Apparent specific dynamic action following feeding and repayment of oxygen debt following anaerobic exercise can each give rise to greater rates of oxygen consumption. Following exhausting exercise there is a delay of about 1 h before oxygen consumption reaches a peak level some 40% higher than the peak level observed during sustained swimming.
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Evidence is building to suggest that both chronic and acute warm temperature exposure, as well as other anthropogenic perturbations, may select for small adult fish within a species. To shed light on this phenomenon, we investigated physiological and anatomical attributes associated with size-specific responses to an acute thermal challenge and a fisheries capture simulation (exercise+air exposure) in maturing male coho salmon (Oncorhynchus kisutch). Full-size females were included for a sex-specific comparison. A size-specific response in haematology to an acute thermal challenge (from 7 to 20 °C at 3 °C h(-1)) was apparent only for plasma potassium, whereby full-size males exhibited a significant increase in comparison with smaller males ('jacks'). Full-size females exhibited an elevated blood stress response in comparison with full-size males. Metabolic recovery following exhaustive exercise at 7 °C was size-specific, with jacks regaining resting levels of metabolism at 9.3 ± 0.5 h post-exercise in comparison with 12.3 ± 0.4 h for full-size fish of both sexes. Excess post-exercise oxygen consumption scaled with body mass in male fish with an exponent of b = 1.20 ± 0.08. Jacks appeared to regain osmoregulatory homeostasis faster than full-size males, and they had higher ventilation rates at 1 h post-exercise. Peak metabolic rate during post-exercise recovery scaled with body mass with an exponent of b~1, suggesting that the slower metabolic recovery in large fish was not due to limitations in diffusive or convective oxygen transport, but that large fish simply accumulated a greater 'oxygen debt' that took longer to pay back at the size-independent peak metabolic rate of ~6 mg min(-1) kg(-1). Post-exercise recovery of plasma testosterone was faster in jacks compared with full-size males, suggesting less impairment of the maturation trajectory of smaller fish. Supporting previous studies, these findings suggest that environmental change and non-lethal fisheries interactions have the potential to select for small individuals within fish populations over time.
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The northern range of Atlantic cod (Gadus morhua), overlaps the southern range of the Greenland cod (Gadus ogac), in the coastal waters of Western Greenland. The availability of a temperate water species (G. morhua) in the same area and oceanographic conditions as a polar species (G. ogac) presented us with the ideal circumstances to test the hypothesis of metabolic cold adaptation (MCA) since many of the problems associated with MCA studies (adaptation of the animals beyond their normal temperature range or mathematical extrapolation of data to common temperatures) could thus be avoided. We therefore used a swim tunnel to measure oxygen consumption in fish at 4C over a range of swimming speeds and following exhaustion, monitored the size of the oxygen debt and time of oxygen debt repayment. There were no significant differences in standard (60–72 mg O2 kg–1 hr–1), routine (76 mg O2 kg–1hr–1), active (137mg O2 kg–1hr–1), or maximal (157 mg O2 kg–1hr–1) metabolic rate, metabolic scope (2.5) or critical swimming speed (2.2 BLs–1) between the two species. Following exhaustive swimming, however, the half-time for oxygen debt repayment in G. ogac (43 min) was almost twice that of G. morhua (25 min). Despite its circumpolar distribution, therefore, there was no evidence of MCA in G. ogac.
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Standard metabolic rate (SMR) and active metabolic rate (AMR) are two fundamental physiological parameters providing the floor and ceiling in aerobic energy metabolism. The total amount of energy available within these two parameters confines constitutes the absolute aerobic scope (AAS). Previous studies on fish have found SMR to closely correlate with dominance and position in the social hierarchy, and to be highly repeatable over time when fish were provided an ad libitum diet. In this study we tested the temporal repeatability of individual SMR, AMR and AAS, as well as repeatability of body mass, in young brown trout (Salmo trutta L.) fed a moderately restricted diet (0.5-0.7% fish mass day⁻¹). Metabolism was estimated from measurements of oxygen consumption rate (M(.)(O₂)) and repeatability was evaluated four times across a 15-week period. Individual body mass was highly repeatable across the entire 15 week experimental period whereas residual body-mass-corrected SMR, AMR and AAS showed a gradual loss of repeatability over time. Individual residual SMR, AMR and AAS were significantly repeatable in the short term (5 weeks), gradually declined across the medium term (10 weeks) and completely disappeared in the long term (15 weeks). We suggest that this gradual decline in repeatability was due to the slightly restricted feeding regime. This is discussed in the context of phenotypic plasticity, natural selection and ecology.
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Metabolic rate has been linked to growth, reproduction, and survival at the individual level and is thought to have far reaching consequences for the ecology and evolution of organisms. However, metabolic rates must be consistent (i.e. repeatable) over at least some portion of the lifetime in order to predict their longer-term effects on population dynamics and how they will respond to selection. Previous studies demonstrate that metabolic rates are repeatable under constant conditions but potentially less so in more variable environments. We measured the standard (= minimum) metabolic rate, maximum metabolic rate, and aerobic scope (= interval between standard and maximum rates) in juvenile brown trout (Salmo trutta) after 5weeks acclimation to each of three consecutive test temperatures (10, 13, and then 16°C) that simulated the warming conditions experienced throughout their first summer of growth. We found that metabolic rates are repeatable over a period of months under changing thermal conditions: individual trout exhibited consistent differences in all three metabolic traits across increasing temperatures. Initial among-individual differences in metabolism are thus likely to have significant consequences for fitness-related traits over key periods of their life history.
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Cytochrome c oxidase (COX), the terminal enzyme of the electron transport system, is central to aerobic metabolism of animals. Many aspects of its structure and function are highly conserved, yet, paradoxically, it is also an important model for studying the evolution of the metabolic phenotype. In this review, part of a special issue honouring Peter Hochachka, we consider the biology of COX from the perspective of comparative and evolutionary biochemistry. The approach is to consider what is known about the enzyme in the context of conventional biochemistry, but focus on how evolutionary researchers have used this background to explore the role of the enzyme in biochemical adaptation of animals. In synthesizing the conventional and evolutionary biochemistry, we hope to identify synergies and future research opportunities. COX represents a rare opportunity for researchers to design studies that span the breadth of biology: molecular genetics, protein biochemistry, enzymology, metabolic physiology, organismal performance, evolutionary biology, and phylogeography.
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We studied the effects of catch-and-release angling on rock bass Ambloplites rupestris a small but common centrarchid species in North America. A field study of hooking injury and mortality was conducted in Lake Erie at a water temperature of 16°C. We captured fish using one of four terminal tackle types: barbless worm, barbed worm, barbless jig, and barbed jig. No mortality was observed in any of the four treatments even after holding fish for 5 d. Fish captured using worms were hooked more deeply than fish caught on jigs. Fish captured on barbless jigs were unhooked most easily and more rapidly than with all other tackle types, resulting in an average of only 20 s of air exposure. Because they were more difficult to remove from the hook, fish captured on other terminal tackle experienced at least twice as much air exposure. To assess sublethal effects, we measured the cardiac responses of rock bass exposed to 30 s of simulated angling followed by 30 or 180 s of air exposure. These air exposure durations were intended to simulate the conditions faced by fish that were either easy or difficult to remove from the hook. Fish experienced arrhythmia during angling, although overall cardiac output increased. Fish experienced severe bradycardia during air exposure, but after being returned to the water, all fish exhibited elevated cardiac output. Fish exposed to 30 s of air exposure required 2 h for full recovery, whereas those exposed to 180 s of air required 4 h. During periods of cardiac disturbance, increases in cardiac output were due to both heightened heart rate and stroke volume. Our results suggest that hooking mortality did not vary with bait or hook type and that physiological disturbance of rock bass was influenced by the duration of air exposure, as influenced by bait and hook choice. We recommend that anglers attempt to minimize handling and air exposure of angled fish and keep pliers or other hook removal devices readily accessible to facilitate rapid release of fish not intended for harvest.
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Accounting for energy use by fishes has been taking place for over 200 years. The original, and continuing gold standard for measuring energy use in terrestrial animals, is to account for the waste heat produced by all reactions of metabolism, a process referred to as direct calorimetry. Direct calorimetry is not easy or convenient in terrestrial animals and is extremely difficult in aquatic animals. Thus, the original and most subsequent measurements of metabolic activity in fishes have been measured via indirect calorimetry. Indirect calorimetry takes advantage of the fact that oxygen is consumed and carbon dioxide is produced during the catabolic conversion of foodstuffs or energy reserves to useful ATP energy. As measuring [CO2] in water is more challenging than measuring [O2], most indirect calorimetric studies on fishes have used the rate of O2 consumption. To relate measurements of O2 consumption back to actual energy usage requires knowledge of the substrate being oxidized. Many contemporary studies of O2 consumption by fishes do not attempt to relate this measurement back to actual energy usage. Thus, the rate of oxygen consumption (M˙O2) has become a measurement in its own right that is not necessarily synonymous with metabolic rate. Because all extant fishes are obligate aerobes (many fishes engage in substantial net anaerobiosis, but all require oxygen to complete their life cycle), this discrepancy does not appear to be of great concern to the fish biology community, and reports of fish oxygen consumption, without being related to energy, have proliferated. Unfortunately, under some circumstances, these measures can be quite different from one another. A review of the methodological history of the two measurements and a look towards the future are included.
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A major challenge for fish biologists in the 21st century is to predict the biotic effects of global climate change. With marked changes in biogeographic distribution already in evidence for a variety of aquatic animals, mechanistic explanations for these shifts are being sought, ones that then can be used as a foundation for predictive models of future climatic scenarios. One mechanistic explanation for the thermal performance of fishes that has gained some traction is the oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis, which suggests that an aquatic organism's capacity to supply oxygen to tissues becomes limited when body temperature reaches extremes. Central to this hypothesis is an optimum temperature for absolute aerobic scope (AAS, loosely defined as the capacity to deliver oxygen to tissues beyond a basic need). On either side of this peak for AAS are pejus temperatures that define when AAS falls off and thereby reduces an animal's absolute capacity for activity. This article provides a brief perspective on the potential uses and limitations of some of the key physiological indicators related to aerobic scope in fishes. The intent is that practitioners who attempt predictive ecological applications can better recognize limitations and make better use of the OCLTT hypothesis and its underlying physiology.
Article
Maximum (aerobic) metabolic rate (MMR) is defined here as the maximum rate of oxygen consumption (M˙O2max ) that a fish can achieve at a given temperature under any ecologically relevant circumstance. Different techniques exist for eliciting MMR of fishes, of which swim-flume respirometry (critical swimming speed tests and burst-swimming protocols) and exhaustive chases are the most common. Available data suggest that the most suitable method for eliciting MMR varies with species and ecotype, and depends on the propensity of the fish to sustain swimming for extended durations as well as its capacity to simultaneously exercise and digest food. MMR varies substantially (>10 fold) between species with different lifestyles (i.e. interspecific variation), and to a lesser extent (<three-fold) between individuals of the same species (i.e. intraspecific variation). MMR often changes allometrically with body size and is modulated by several environmental factors, including temperature and oxygen availability. Due to the significance of MMR in determining aerobic scope, interest in measuring this trait has spread across disciplines in attempts to predict effects of climate change on fish populations. Here, various techniques used to elicit and measure MMR in different fish species with contrasting lifestyles are outlined and the relevance of MMR to the ecology, fitness and climate change resilience of fishes is discussed.
Article
Because of its profound effects on the rates of biological processes such as aerobic metabolism, environmental temperature plays an important role in shaping the distribution and abundance of species. As temperature increases, the rate of metabolism increases and then rapidly declines at higher temperatures - a response that can be described using a thermal performance curve (TPC). Although the shape of the TPC for aerobic metabolism is often attributed to the competing effects of thermodynamics, which can be described using the Arrhenius equation, and the effects of temperature on protein stability, this account represents an over-simplification of the factors acting even at the level of single proteins. In addition, it cannot adequately account for the effects of temperature on complex multistep processes, such as aerobic metabolism, that rely on mechanisms acting across multiple levels of biological organization. The purpose of this review is to explore our current understanding of the factors that shape the TPC for aerobic metabolism in response to acute changes in temperature, and to highlight areas where this understanding is weak or insufficient. Developing a more strongly grounded mechanistic model to account for the shape of the TPC for aerobic metabolism is crucial because these TPCs are the foundation of several recent attempts to predict the responses of species to climate change, including the metabolic theory of ecology and the hypothesis of oxygen and capacity-limited thermal tolerance. © 2015. Published by The Company of Biologists Ltd.
Article
In many fisheries, some component of the catch is usually released. Quantifying the effects of capture and release on fish survival is critical for determining which practices are sustainable, particularly for threatened species. Using a standardized fishing technique, we studied sublethal (blood physiology and reflex impairment assessment) and lethal (post-release mortality with satellite tags) outcomes of fishing stress on 5 species of coastal sharks (great hammerhead, bull, blacktip, lemon, and tiger). Species-specific differences were detected in whole blood lactate, partial pressure of carbon dioxide, and pH values, with lactate emerging as the sole parameter to be significantly affected by increasing hooking duration and shark size. Species-specific differences in reflex impairment were also found; however, we did not detect any significant relationships between reflex impairment and hooking duration. Taken together, we ranked each species according to degree of stress response, from most to least disturbed, as follows: hammerhead shark > blacktip shark > bull shark > lemon shark > tiger shark. Satellite tagging data revealed that nearly 100% of all tracked tiger sharks reported for at least 4 wk after release, which was significantly higher than bull (74.1%) and great hammerhead (53.6%) sharks. We discuss which mechanisms may lead to species-specific differences in sensitivity to fishing and suggest that observed variation in responses may be influenced by ecological and evolutionary phenomena. Moreover, our results show that certain species (i.e. hammerhead sharks in this study) are inherently vulnerable to capture stress and mortality resulting from fisheries interactions and should receive additional attention in future conservation strategies.
Article
Equatorial populations of marine species are predicted to be most impacted by global warming because they could be adapted to a narrow range of temperatures in their local environment. We investigated the thermal range at which aerobic metabolic performance is optimum in equatorial populations of coral reef fish in northern Papua New Guinea. Four species of damselfishes and two species of cardinal fishes were held for 14 days at 29, 31, 33, and 34 °C, which incorporated their existing thermal range (29-31 °C) as well as projected increases in ocean surface temperatures of up to 3 °C by the end of this century. Resting and maximum oxygen consumption rates were measured for each species at each temperature and used to calculate the thermal reaction norm of aerobic scope. Our results indicate that one of the six species, Chromis atripectoralis, is already living above its thermal optimum of 29 °C. The other five species appeared to be living close to their thermal optima (ca. 31 °C). Aerobic scope was significantly reduced in all species, and approached zero for two species at 3 °C above current-day temperatures. One species was unable to survive even short-term exposure to 34 °C. Our results indicate that low-latitude reef fish populations are living close to their thermal optima and may be more sensitive to ocean warming than higher-latitude populations. Even relatively small temperature increases (2-3 °C) could result in population declines and potentially redistribution of equatorial species to higher latitudes if adaptation cannot keep pace.
Article
Ten years research on metabolic rates and swimming speeds of sockeye salmon (Oncorhynchus nerka) ranging in weight from 2 to 2000 g, at temperatures from 2 to 24 C, is reviewed and summarized. Analysis of weight–slope relations (b values) at three temperatures, using log–log transformations, provided an overall mean of 0.88 for standard metabolism and 0.99 for active metabolism. A previously determined semilog equation for temperature effect on standard metabolic rate (at approximately 50 g) was supported by supplementary data at 2 C. Predictive graphic models in the form of isopleths of metabolic rates and critical swimming speeds in relation to weight, length, and temperature are depicted. These provide a composite presentation useful in estimating the metabolic rate and maximum sustained speed for any size and temperature.
Article
The rate of oxygen consumption in young sockeye salmon (Oncorhynchus nerka) was determined for various swimming speeds, including fatigue levels, at temperatures of 5, 10, 15, 20, and 24 °C. A logarithmic increase in oxygen demand with increase in swimming speed characterized each acclimation temperature. Extrapolation to zero activity (standard metabolism) and maximum activity (active metabolism) provided differences of the order of 10 to 12 times the minimum rate.The greatest scope for activity occurred at 15 °C with an average active metabolic rate of 895 mg O2/kg/hr for a swimming speed of 4.1 body lengths per second, just maintained for 1 hr. Above 15 °C active metabolism was limited, apparently by oxygen availability.Rate of replacement of oxygen debt following fatigue was determined by tracing the return to a resting state of metabolism, and confirmed by re-tests at fatigue velocities. In most instances the rate declined logarithmically with time; in some there was an initial or secondary slump. Times to recovery (return of spontaneous activity) averaged 3.2 hr, independent of acclimation temperature.Swimming speed–fatigue tests indicated a sustained level of performance at about 200–300 min. Comparison with other fish suggests a marked change in slope of the fatigue curve at about 20 sec. The effect of temperature was greatest on sustained speeds and least on burst speeds.
Article
The resting oxygen consumption , postprandial and post-exercise peak oxygen consumption of 137 juvenile southern catfish Silurus meridionalis, weighing 18·5 ± 0·8 g (mean ±s.d.), were measured at 25° C to determine whether is positively related to postprandial and post-exercise in sedentary S. meridionalis. In addition, postprandial metabolic response [i.e. the specific dynamic action (SDA)] after a satiating meal and the growth performance as a consequence of a 3 week feeding-growth trail were measured in 40 S. meridionalis, weighing 14·3 ± 0·2 g, at 25° C to determine whether postprandial is positively related to growth rate. Postprandial was positively correlated with , while post-exercise was not. Both postprandial and post-exercise were positively correlated with factorial and absolute scope. There was no significant correlation between the growth rate and postprandial in S. meridionalis. It suggested that as a sit-and-wait forager with low , low post-exercise and high postprandial , the expenditure of energy for maintenance in S. meridionalis may be more closely related to digestive processes than locomotor activities.
Article
This study tests whether or not post-exercise oxygen consumption rates (Mo2) in fish are dependent upon how exhaustion is induced. A group of eight Atlantic cod (Gadus morhua) were each exercised using (1) a critical swimming speed (Ucrit) protocol, (2) an exercise protocol designed to measure anaerobic capacity of fish (Uburst), and (3) a protocol in which the fish were chased to exhaustion manually. Mo2 was measured for a 2-h period following exhaustion induced by all three exercise regimes (Ucrit, Uburst and chase). Post-exercise Mo2 following exhaustion from the Uburst and chase protocols were significantly higher than post-exercise Mo2 following the Ucrit protocol. Each fish during the Ucrit protocol exhibited maximal Mo2 during exercise rather than during recovery, yet 75% of the fish during Ubrust recovery and 100% during chase recovery exhibited Mo2 higher than that measured during Ucrit exercise. These results, as well as the large interindividual variations in Mo2 among the eight fish, show that post-exhaustion Mo2 is specific to the exercise regime employed, thus, investigators must exercise caution when combining results from different exercise protocols and/or individuals.
Article
Standard metabolic rate (SMR), active metabolic rate (AMR) and critical oxygen saturation (Scrit) were measured in Atlantic cod Gadus morhua at 5, 10 and 15° C. The SMR was 35.5, 57.0 and 78.2 mg O2 kg−1 h−1 and Scrit was 16.5, 23.2 and 30.3%, at 5, 10 and 15° C, respectively. Previously reported SMR for Atlantic cod from arctic waters at 4° C was twice that measured at 5° C in the present study. A possible intraspecific latitudinal difference in the SMR is discussed. The AMR was 146.6, 197.9 and 200.4 mg O2 kg−1 h−1 and the critical swimming speed (Ucrit) was 1 6, 1.7 and 1.9 at 5, 10 and 15° C, respectively. The maximum oxygen consumption was found to be associated with exercise, rather than recovery from exercise as previously reported in another Study of Cod metabolism.
Article
Atlantic cod (Gadus morhua) were forced to swim in a swim tunnel respirometer until fatigued; oxygen consumption rate (ṀO2) was measured during swimming at incremental speeds until the fish was exhausted and during recovery from exhaustion. Maximal oxygen consumption (ṀO2max) occurred during maximal activity as has been found for other fish species, but at odds with the current paradigm for Atlantic cod. Earlier experiments had drawn the conclusion that ṀO2max in Atlantic cod occurs during recovery from exhaustive exercise. We found no support for this paradigm in our experiments and we propose that the respiratory physiology of Atlantic cod is not unlike that of other fishes.
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ATPases involved in ion translocation are present in a diverse variety of biological membranes. Three major classes of these ‘ion motive’ enzymes, designated here as ‘P’ (phosphorylated), ‘V’ (vacuolar), and ‘F’ (F0F1), are now known to exist. In addition to the regulation of intracellular ionic or pH balance, some ATPases help drive numerous physiological or biological processes by ‘energy coupling’. Among these are muscle relaxation, receptor recycling, hormone storage, food digestion and ATP synthesis. A number of laboratories are now trying to identify individual steps of ATPase reaction pathways, while others are endeavouring to identify those ‘genetic codes’ responsible for the energy coupling events.
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The relationship between metabolic rate of pike (Y, mgO2) and body weight (X, g) over the range 40–1291 gat 15° C is of the form: Y=aXb. For resting metabolic rate (Vo2, rest), the scaling coefficient, b, is 0.80 and for maximum metabolic rate measured after exhaustive swimming (V02, max), b is 0.99. Factorial metabolic scope (V02, max/ V02, rest) increases with body weight. Peak postprandial oxygen consumption (V02, ASDA) is a constant multiple of V02 rest for any discrete meal (expressed as % of body weight) up to 10% body weight. V02ASDA after a single meal can utilize the entire metabolic scope (V02, max—V02, rest) of juvenile but not adult pike.
Article
1 Although the repeatability of a trait is of interest for several reasons, few studies have critically examined the repeatability or correlation of metrics of swimming performance. We quantified repeatability of three swimming performances (burst speed during a c-start escape response, critical swimming speed [Ucrit], maximum speed [Umax]) and size/shape measures over short (within-day), medium (days and weeks), and long (more than a year) time-scales in a small poeciliid fish, the Trinidadian guppy (Poecilia reticulata).
Article
Novel field measurements of critical swimming speed (Ucrit) and oxygen uptake ( Mo2) in three species of adult Pacific salmon Oncorhynchus spp. up to 3·5 kg in body mass were made using two newly designed, mobile Brett-type swim tunnel respirometers sited at a number of field locations in British Columbia, Canada. Measurements of Ucrit, which ranged from 1· 68 to 2·17 body lengths s−1, and maximum Mo2, which ranged from 8·74 to 12·63 mg O2 kg−1 min−1 depending on the species and field location, were judged to be of similar quality when compared with available data for laboratory-based studies. Therefore high quality respirometry studies were possible in the field using adult wild swimming salmonids. In addition, the recovery of wild adult Pacific salmon from the exhaustive Ucrit swim test was sufficiently rapid that swimming performance could be repeated with <1 h of recovery time between the termination of the initial swim test and the start of the second test. Moreover, this repeat swimming performance was possible without routine Mo2 being reestablished. This result suggests that wild adult salmon are capable of carrying a moderate excess post-exercise oxygen consumption without adversely affecting Ucrit, maximum Mo2 or swimming economy. Such capabilities may be extremely important for timely migratory passages when salmonids face repetitive hydraulic challenges on their upstream migration.
Article
Energy balance is a fundamental requirement of stress adaptation and tolerance. We explore the links between metabolism, energy balance and stress tolerance using aquatic invertebrates as an example and demonstrate that using key parameters of energy balance (aerobic scope for growth, reproduction and activity; tissue energy status; metabolic rate depression; and compensatory onset of anaerobiosis) can assist in integrating the effects of multiple stressors and their interactions and in predicting the whole-organism and population-level consequences of environmental stress. We argue that limitations of both the amount of available energy and the rates of its acquisition and metabolic conversions result in trade-offs between basal maintenance of a stressed organism and energy costs of fitness-related functions such as reproduction, development and growth and can set limit to the tolerance of a broad range of environmental stressors. The degree of stress-induced disturbance of energy balance delineates transition from moderate stress compatible with population persistence (pejus range) to extreme stress where only time-limited existence is possible (pessimum range). It also determines the predominant adaptive strategy of metabolic responses (energy compensation vs. conservation) that allows an organism to survive the disturbance. We propose that energy-related biomarkers can be used to determine the conditions when these metabolic transitions occur and thus predict ecological consequences of stress exposures. Bioenergetic considerations can also provide common denominator for integrating stress responses and predicting tolerance limits under the environmentally realistic scenarios when multiple and often variable stressors act simultaneously on an organism. Determination of bioenergetic sustainability at the organism's level (or lack thereof) has practical implications. It can help identify the habitats and/or conditions where a population can survive (even if at the cost of reduced reproduction and growth) and those that are incapable of supporting viable populations. Such an approach will assist in explaining and predicting the species' distribution limits in the face of the environmental change and informing the conservation efforts and resource management practices.
Article
The mean ±s.e. optimum temperature (T(opt)) for aerobic scope in juvenile coho salmon Oncorhynchus kisutch was determined to be 17·0 ± 0·7° C. The repeated measures protocol took 3 weeks to complete the T(opt) determination using 12 fish tested at five temperatures separated by 2° C increments. This experiment also demonstrated that the T(opt) was associated with maximum heart rate (f(H)) failing to maintain a Q(10) -related increase with temperature. When maximum f(H) was produced in anaesthetized fish with pharmacological stimulation and f(H) measured from electrocardiogram recordings during acute warming, the Arrhenius break temperature (ABT) for Q(10) discontinuities in maximum f(H) (mean ±s.e. = 17·1 ± 0·5° C for 15 ppm clove oil and 16·5 ± 0·2° C for 50 ppm MS-222) was statistically indistinguishable from the T(opt) measured using aerobic scope. Such a determination took only 3 days rather than 3 weeks. Therefore, it is proposed that determining ABT for discontinuities in maximum f(H) in anaesthetized fish presents itself as a valuable, high-throughput screening tool to assess T(opt) in fishes, a metric that has become recognized as being extremely valuable in fish biology and fisheries management.