Pairing lab and field studies to predict thermal performance of wild fish.

In thermally variable ecosystems, temperatures can change extensively on hourly and seasonal timescales requiring ectotherms to possess a broad thermal tolerance (critical thermal minima [CTmin] and maxima [CTmax]). However, whether fish acclimate in the laboratory similarly as they acclimatize in the field under comparable thermal variation is unclear. We used temperature data from a tidal salt marsh to design 21-day lab-acclimation treatments (static: 12, 17, 22, 27 °C; daily variation with mean 22 °C: i) range 17-27 °C, ii) range 17-27 °C with irregular extremes within 12-32 °C). We compared thermal limits in lab-acclimated and field-acclimatized eurythermal arrow goby (Clevelandia ios). Variable temperature-acclimated and acclimatized fish had similar CTmin and CTmax. Notably, arrow gobies showed rapid plasticity in their absolute thermal tolerance within one tidal cycle. The daily mean and max temperatures experienced were positively related to CTmax and CTmin, respectively. This study demonstrates that ecologically informed lab acclimation treatments can yield tolerance results that are applicable to wild fish.

Body size and temperature affect metabolic and cardiac thermal tolerance in fish.

Environmental warming is associated with reductions in ectotherm body sizes, suggesting that larger individuals may be more vulnerable to climate change. The mechanisms driving size-specific vulnerability to temperature are unknown but are required to finetune predictions of fisheries productivity and size-structure community responses to climate change. We explored the potential metabolic and cardiac mechanisms underlying these body size vulnerability trends in a eurythermal fish, barred surfperch. We acutely exposed surfperch across a large size range (5-700 g) to four ecologically relevant temperatures (16 °C, 12 °C, 20 °C, and 22 °C) and subsequently, measured their metabolic capacity (absolute and factorial aerobic scopes, maximum and resting metabolic rates; AAS, FAS, MMR, RMR). Additionally, we estimated the fish's cardiac thermal tolerance by measuring their maximum heart rates (fHmax) across acutely increasing temperatures. Barred surfperch had parallel hypoallometric scaling of MMR and RMR (exponent 0.81) and a weaker hypoallometric scaling of fHmax (exponent - 0.05) across all test temperatures. In contrast to our predictions, the fish's aerobic capacity was maintained across sizes and acute temperatures, and larger fish had greater cardiac thermal tolerance than smaller fish. These results demonstrate that thermal performance may be limited by different physiological constraints depending on the size of the animal and species of interest.

Intraspecific variability in thermal tolerance: a case study with coastal cutthroat trout.

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.

Diet mediates thermal performance traits: implications for marine ectotherms.

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 with 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.

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

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.

Hypoxia tolerance is unrelated to swimming metabolism of wild, juvenile striped bass (Morone saxatilis).

Juvenile striped bass residing in Chesapeake Bay are likely to encounter hypoxia that could affect their metabolism and performance. The ecological success of this economically valuable species may depend on their ability to tolerate hypoxia and perform fitness-dependent activities in hypoxic waters. We tested whether there is a link between hypoxia tolerance (HT) and oxygen consumption rate (MO2 ) of juvenile striped bass measured while swimming in normoxic and hypoxic water, and to identify the interindividual variation and repeatability of these measurements. HT (loss of equilibrium) of fish (N=18) was measured twice collectively, 11 weeks apart, between which MO2  was measured individually for each fish while swimming in low flow (10.2 cm s-1) and high flow (∼67% of critical swimming speed, Ucrit) under normoxia and hypoxia. Both HT and MO2  varied substantially among individuals. HT increased across 11 weeks while the rank order of individual HT was significantly repeatable. Similarly, MO2  increased in fish swimming at high flow in a repeatable fashion, but only within a given level of oxygenation. MO2  was significantly lower when fish were swimming against high flow under hypoxia. There were no clear relationships between HT and MO2  while fish were swimming under any conditions. Only the magnitude of increase in HT over 11 weeks and an individual's MO2  under low flow were correlated. The results suggest that responses to the interacting stressors of hypoxia and exercise vary among individuals, and that HT and change in HT are not simple functions of aerobic metabolic rate.

Strong Evidence for an Intraspecific Metabolic Scaling Coefficient Near 0.89 in Fish.

As an example of applying the evidential approach to statistical inference, we address one of the longest standing controversies in ecology, the evidence for, or against, a universal metabolic scaling relationship between metabolic rate and body mass. Using fish as our study taxa, we curated 25 studies with measurements of standard metabolic rate, temperature, and mass, with 55 independent trials and across 16 fish species and confronted this data with flexible random effects models. To quantify the body mass - metabolic rate relationship, we perform model selection using the Schwarz Information Criteria (ΔSIC), an established evidence function. Further, we formulate and justify the use of ΔSIC intervals to delineate the values of the metabolic scaling relationship that should be retained for further consideration. We found strong evidence for a metabolic scaling coefficient of 0.89 with a ΔSIC interval spanning 0.82 to 0.99, implying that mechanistically derived coefficients of 0.67, 0.75, and 1, are not supported by the data. Model selection supports the use of a random intercepts and random slopes by species, consistent with the idea that other factors, such as taxonomy or ecological or lifestyle characteristics, may be critical for discerning the underlying process giving rise to the data. The evidentialist framework applied here, allows for further refinement given additional data and more complex models.

Repeatability of Hypoxia Tolerance of Individual Juvenile Striped Bass Morone saxatilis and Effects of Social Status.

Chesapeake Bay is the primary nursery for striped bass (Morone saxatilis), which are increasingly being exposed to hypoxic waters. Tolerance to hypoxia in fish is generally determined by a single exposure of an isolated individual or by exposing large groups of conspecifics to hypoxia without regard to social status. The importance of social context in determining physiological responses to stressors is being increasingly recognized. To determine whether social interactions influence hypoxia tolerance (HT) in striped bass, loss of equilibrium HT was assessed in the same fish while manipulating the social environment around it. Small group settings were used to be more representative of the normal sociality experienced by this species than the paired encounters typically used. After establishing the dominance hierarchy within a group of fish, HT was determined collectively for the individuals in that group, and then new groups were constructed from the same pool of fish. Individuals could then be followed across multiple settings for both repeatability of HT and hierarchy position ( X¯=4.2±0.91 SD groups per individual). HT increased with repeated exposures to hypoxia ( P<0.001 ), with a significant increase by a third exposure ( P=0.004 ). Despite this changing HT, rank order of HT was significantly repeatable across trials for 6 mo ( P=0.012 ). Social status was significantly repeatable across trials of different group composition ( P=0.02 ) and unrelated to growth rate but affected HT weakly in a complex interaction with size. Final HT was significantly correlated with blood [hemoglobin] and hematocrit. The repeatability and large intraspecific variance of HT in juvenile striped bass suggest that HT is potentially an important determinant of Darwinian fitness in an increasingly hypoxic Chesapeake Bay.

Hypoxia and Sprint Swimming Performance of Juvenile Striped Bass, Morone saxatilis.

Annual hypoxia in the Chesapeake Bay has expanded to the point where Darwinian fitness of juvenile striped bass (Morone saxatilis) may depend on their ability to perform in low-oxygen environments. The locomotion they use in predator/prey dynamics relies primarily on white (type II) muscle that is powered by anaerobic metabolic pathways and has generally been thought to be immune to aquatic hypoxia. We tested the sprint performance of 15 juvenile striped bass twice under acute hypoxia (20% air saturation [AS]) 5 wk apart and once under normoxia (>85% AS) in between. Average sprint performance was lower under the first hypoxia exposure than in normoxia and increased in the second hypoxia test relative to the first. The rank order of individual sprint performance was significantly repeatable when comparing the two hypoxia tests but not when compared with sprint performance measured under normoxic conditions. The maximum sprint performance of each individual was also significantly repeatable within a given day. Thus, sprint performance of striped bass is reduced under hypoxia, is phenotypically plastic, and improves with repetitive hypoxia exposures but is unrelated to relative sprint performance under normoxia. Since energy to fuel a sprint comes from existing ATP and creatine phosphate stores, the decline in sprint performance probably reflects reduced function of a part of the reflex chain leading from detection of aversive stimuli to activation of the muscle used to power the escape response.