The metabolic index concept combines metabolic data and known thermal sensitivities to estimate the factorial aerobic scope of animals in different habitats, which is valuable for understanding the metabolic demands that constrain species' geographical distributions. An important assumption of this concept is that the O2 supply capacity (which is equivalent to the rate of oxygen consumption divided by the environmental partial pressure of oxygen: ) is constant at O2 tensions above the critical O2 threshold (i.e. the where O2 uptake can no longer meet metabolic demand). This has led to the notion that hypoxia vulnerability is not a selected trait, but a by-product of selection on maximum metabolic rate. In this Commentary, we explore whether this fundamental assumption is supported among fishes. We provide evidence that O2 supply capacity is not constant in all fishes, with some species exhibiting an elevated O2 supply capacity in hypoxic environments. We further discuss the divergent selective pressures on hypoxia- and exercise-based cardiorespiratory adaptations in fishes, while also considering the implications of a hypoxia-optimized O2 supply capacity for the metabolic index concept.

Global oceans and other aquatic habitats are changing at unprecedented rates as a result of natural and anthropogenic forces driving climate change. These changes include ocean warming, deoxygenation and acidification, all of which have been the subject of intense study by marine biologists in recent years (e.g. Keeling et al., 2010; Bozinovic and Portner, 2015; Esbaugh, 2018). Much of this work has focused on identifying and understanding the physiological traits that confer tolerance and sensitivity to environmental changes in different species. From a physiological perspective, there has been particular focus on respiratory performance, as all three climate change stressors pose specific challenges to respiratory gas transport. Respiratory performance is often quantified through the determination of aerobic scope (AS; see Glossary), which is the difference between the baseline cost of living (i.e. standard metabolic rate, SMR; see Glossary) and the maximum capacity to transport oxygen from the environment to mitochondria (maximum metabolic rate, MMR; see Glossary) (Clark et al., 2013). AS has become an important ecophysiological metric because it quantifies all the energy available for non-vital functions such as activity, reproduction and growth. Environmental stressors can act as either ‘limiting’ or ‘loading’ stressors that constrain oxygen (O2) supply or raise metabolic costs, respectively.

List of symbols and abbreviations

     
  • AS

    aerobic scope

  •  
  • the difference in arterial and venous blood oxygen content

  •  
  • CTmax

    the upper temperature limit for a species

  •  
  • ED

    the thermal sensitivity of oxygen demand

  •  
  • EO

    the thermal sensitivity of hypoxia vulnerability (i.e. Pcrit)

  •  
  • ES

    the thermal sensitivity of oxygen supply (i.e. MMR)

  •  
  • FAS

    factorial aerobic scope

  •  
  • MMR

    maximum metabolic rate

  •  
  • oxygen consumption rate

  •  
  • Pcrit

    critical oxygen threshold

  •  
  • Pcrit,max

    the critical oxygen threshold for maximum metabolic rate

  •  
  • SMR

    standard metabolic rate

  •  
  • Vb

    cardiac output

  •  
  • αD

    oxygen demand (i.e. standard metabolic rate)

  •  
  • αS

    oxygen supply capacity

  •  
  • ɸ

    the metabolic index

  •  
  • ɸ­crit

    the metabolic index found at the equatorial or depth limit of a species distribution

Glossary

Aerobic scope

The energy available for all non-vital functions.

Bradycardia

A reduced heart rate.

Cardiac output

The volume of blood pumped by the heart per unit time.

Cardiac power

The ability of the heart to generate output against pressure.

Critical oxygen threshold

A measure of hypoxia vulnerability. The partial pressure of oxygen where oxygen uptake can no longer meet the requirements of standard metabolic rate.

Critical oxygen threshold maximum

A measure of the effects of reduced oxygen on maximum metabolic rate. The partial pressure of oxygen that causes a decline in maximum metabolic rate.

Factorial aerobic scope

The energy available for all non-vital functions expressed as the ratio of maximum metabolic rate to standard metabolic rate.

Maximum metabolic rate

The maximum oxygen consumption rate available to an individual during exhaustive exercise.

Metabolic index

The ratio of oxygen supply to demand after accounting for thermal sensitivities and environmental .

Oxygen- and capacity-limited thermal tolerance

A theory that suggests critical thermal limitations of aquatic ectotherms are due to a collapse of aerobic scope.

Oxygen supply capacity

The ratio of maximum oxygen consumption rate to ambient .

Root effect

The tendency of fish hemoglobin to exhibit reduced carrying capacity of O2 at low pH.

Standard metabolic rate

The oxygen consumption rate required to meet the energetic costs of vital physiological functions.

Tachycardia

An elevated heart rate.

Thermal sensitivity

Describes the degree of change in a metabolic trait (e.g. SMR, MMR, Pcrit) as a consequence of warming, expressed by an exponential Arrhenius function.

The global scope of climate change has pushed researchers to seek broad-scale unifying approaches to assess the effects on species' performance and biogeography (i.e. latitudinal shifts in species distribution), the most recent of which is the metabolic index concept (see Glossary; Deutsch et al., 2015; Deutsch et al., 2020). This concept estimates the energy available to aquatic ectotherms (i.e. the metabolic index, ɸ) under varying environmental conditions using the thermal sensitivities of O2 supply and demand, as well as the effects of O2 partial pressure () on O2 supply. This concept has been used to estimate the energy available to aquatic ectotherms at equatorial and depth range limits, providing important information on the possible energetic limitations at these geographic boundaries (Deutsch et al., 2015; Deutsch et al., 2020). Notably, energetic limitations are not based on baseline costs of living (i.e. SMR), but instead are the cumulative result of baseline and routine activity costs across a wide variety of aquatic ectotherms. Approaches such as the metabolic index concept are critical to allow us to understand and predict the effects of climate change on ecosystems. However, it is equally important to critically evaluate whether these concepts are truly universal, and to identify species that may require alternative approaches. This seems particularly important for fishes, which are the most diverse vertebrate group on the planet and which occupy a plethora of different environments and ecological niches (Ravi and Venkatesh, 2008; Nelson et al., 2016). In this Commentary, we ask whether the metabolic index concept, in its current iteration, can be effectively applied to all fish species. Specifically, we seek to examine whether O2 supply capacity (see Glossary) of fishes is constant across O2 partial pressures, and whether it may be optimized to offset hypoxia vulnerability in some species.

Obtaining O2 is a fundamental physiological challenge for fish because of its naturally low solubility in water. Pioneering work by Fry and Hart (1948) demonstrated that warming exacerbates this challenge by simultaneously raising SMR and constraining MMR when temperatures surpass a species' thermal optimum (Fig. 1A). These findings were used as the mechanistic basis for the O2- and capacity-limited thermal tolerance (OCLTT) hypothesis (see Glossary), which is a unifying conceptual framework used to predict the impacts of climate change on aquatic ectotherms (Portner and Knust, 2007; Pörtner and Farrell, 2008; Portner, 2010). Although the OCLTT remains a source of debate (e.g. Jutfelt et al., 2018), in part because not all aquatic ectotherms exhibit O2-dependent thermal limitations (Ern et al., 2016; Ern et al., 2017), the underlying mechanism of observed thermal constraints on MMR are supported in many species (e.g. Fry and Hart, 1948; McBryan et al., 2013; Lefevre, 2016; Slesinger et al., 2019). The metabolic index concept can be considered a refinement of the OCLTT that focuses on AS the determinative endpoint, as opposed to the critical thermal maximums (i.e. CTmax). This concept attempts to explain biogeographical patterns based on respiratory traits and the thermal sensitivity of those traits (Deutsch et al., 2015; Deutsch et al., 2020). The formula for a species' metabolic index (ɸ) is:
formula
(1)
where αS is O2 supply capacity, αD is O2 demand (i.e. SMR), βε is body mass and the associated metabolic scaling coefficient, is the environmental O2 partial pressure, kB is the Boltzmann constant, EO is the temperature sensitivity of hypoxia vulnerability (i.e. the critical oxygen threshold, Pcrit; see Glossary), and T and Tref are temperature and reference temperature (i.e. the temperature where metabolic traits were measured), respectively (Deutsch et al., 2015; Deutsch et al., 2020). Although it is complex, this formula can be thought of as a variation on factorial AS (FAS; see Glossary) that incorporates thermal sensitivity and O2 availability. More simply, ɸ=FAS under normoxia at the reference temperature. Importantly, ɸ only addresses hypoxia vulnerability using Pcrit, which is an aerobic trait that defines the at which an animal can no longer maintain SMR and where AS falls to zero. One important assumption behind the ɸ concept is that αS is constant across . From a physiological perspective, this would mean that the O2 supply constraints that limit O2 uptake in exercising fish at high  are similar to those that limit O2 uptake in resting fish at Pcrit. A second assumption is that the thermal sensitivity of Pcrit (EO) represents the cumulative effects of temperature on O2 supply (ES) and demand (ED) (i.e. EO= EDES). In other words, the Pcrit of a fish at a given temperature is the product of the cumulative thermal constraints on αD and αS, the latter of which can be defined using MMR (i.e. when ). Furthermore, it is assumed that the natural log of thermal sensitivities is linear across the entire thermal range of a species. Below, we consider the validity of these assumptions for fishes in more detail.

The metabolic index concept defines αS as the O2 consumption rate divided by at which the O2 consumption was measured. This can be measured as SMR/Pcrit (Seibel and Deutsch, 2020). The effect of on O2 consumption, and thus αS, is generally described in one of two ways (Fig. 1B). Firstly, through a classical description of the line of O2 limitation, which is often hyperbolic (e.g. Fry, 1947; McBryan et al., 2013; Claireaux and Chabot, 2016). Secondly, and more recently, models have described a linear relationship followed by a plateau (e.g. Wood, 2018; Seibel and Deutsch, 2020). The breakpoint is defined as the Pcrit,max (see Glossary), the below which MMR is constrained. A comprehensive assessment of Pcrit,max across a variety of animal phyla, including mollusks, arthropods and chordates, was recently performed by Seibel and Deutsch (2020), which used available SMR, MMR and Pcrit values to predict Pcrit,max (Pcrit,max=MMR×Pcrit/SMR) in a variety of species from different phyla. Of the 52 species tested – 28 of which were fish – 73% demonstrated a Pcrit,max of approximately 21 kPa O2. This led to the suggestion that hypoxia tolerance, as defined by Pcrit, is simply a by-product of selective pressures on MMR (Seibel and Deutsch, 2020). This conclusion was based on the premise that maximizing MMR and AS in normoxia is a prominent evolutionary driver of respiratory performance and ecological success in aquatic ectotherms. If αS is similar at Pcrit and Pcrit,max, then it is logical to suggest that hypoxia tolerance as defined by Pcrit is a by-product of the evolutionary pressures on MMR. This is probably true for those species with a Pcrit,max of 21 kPa; however, it is less certain for the other 27% of species.

Seibel and Deutsch (2020) suggested that species with a Pcrit,max below approximately 21 kPa are adapted to hypoxic environments, but argue that adaptations to these environments are based on maximizing αS at Pcrit,max (i.e. maximizing MMR). However, this conclusion was reached by extrapolating only a single measurement of αS (i.e. SMR/Pcrit) per species to the measured MMR of that species. Here, we compiled datasets from seven different fish species that allow the calculation of αS across a range (MMR/; Fig. 2; Table S1). These seven species have Pcrit,max values that range from 8.35 to 17.2 kPa, and Pcrit values that range from 2.3 to 6.2 kPa. Of these seven, the red drum (Sciaenops ocellatus) (Ackerly and Esbaugh, 2020) and pumpkinseed (Lepomis gibbosus) (Crans et al., 2015) generally follow the pattern of a constant αS until Pcrit,max. In contrast, four of the species – the largemouth bass (Micropterus salmoides), rock bass (Ambloplites rupestris), blue gill (Lepomis macrochirus) (Crans et al., 2015) and common sole (Solea solea) (Lefrancois and Claireaux, 2003) – deviate from the described pattern with a gradual decline in αS as increases from Pcrit. The pattern of the last species, the black-axil chromis (Chromis atripectoralis) (Ern et al., 2017), is ambiguous but it is included for completeness. All four species without a constant αS have at least one data point between Pcrit and Pcrit,max (Fig. 2). The physiological explanation for the patterns described above is uncertain. It is possible that fish species with a calculated Pcrit,max below 21 kPa have an αS that is selected for specifically on the basis of hypoxia tolerance (i.e. αS at Pcrit), not based on MMR at Pcrit,max. Regardless of the mechanism, it is clear that αS should not be assumed to be constant across values in all fishes.

As discussed above, the available data suggest that αS is not constant across levels in all fish, which suggests that species exhibit an αS that is optimized for performance under either hypoxia or exercise. Here, we will consider whether this dichotomy is consistent with our current understanding of respiratory physiology in fishes. For fish, exercise has often been grouped with other biotic factors such as anemia, acidosis and changes in gill structure that cause ‘functional hypoxia’ (Farrell and Richards, 2009). Although this observation is true in a general sense, the question we will address here is whether there is a mechanistic basis to assume that exercise-induced hypoxia and acute environmentally derived hypoxia are similar from a physiological perspective, and whether there is reason to believe that separate selective pressures can shape exercise performance and hypoxia tolerance (see Table 1). We will use the Fick equation as a functional framework:
formula
(2)
where refers to metabolic O2 consumption, Vb is cardiac output (see Glossary) and is the difference between arterial and venous O2 content. At rest, fish in hypoxia maintain (Fry, 1947; Holeton and Randall, 1967; Negrete and Esbaugh, 2019), whereas exercising fish increase (e.g. Kiceniuk and Jones, 1977; Norin and Clark, 2016). These different challenges necessitate that fish make distinct changes to their cardiorespiratory system by manipulating Vb and to meet O2 demand. Note that this is not intended as a comprehensive review of hypoxia, exercise or cardiorespiratory physiology, as such reviews can be found elsewhere (e.g. Farrell et al., 2009; Gamperl and Driedzic, 2009; Richards, 2011; Eliason and Farrell, 2016).

The first component of the Fick equation is cardiac output, which is a combination of heart rate and stroke volume and refers to the total amount of blood pumped by the heart per unit time. When fish are exposed to hypoxia, they respond with a series of physiological adjustments intended to maintain O2 delivery to the heart and brain. In most fishes, hypoxia exposure causes significant bradycardia (see Glossary) accompanied by increased stroke volume (Farrell, 2007; Gamperl and Driedzic, 2009) stimulated by elevated venous pressure (Sandblom and Axelsson, 2005) – although, in some species, this response does not occur until the fish approaches Pcrit (e.g. Atlantic cod, Gadhus morhua) (McKenzie et al., 2009; Petersen and Gamperl, 2011). The observed change in cardiac output under hypoxia depends on whether increased stroke volume fully compensates for the bradycardia (Farrell, 2007; Gamperl and Driedzic, 2009). In some species, such as Adriatic sturgeon (Acipenser naccarii; Agnisola et al., 1999) and rainbow trout (Oncorhynchus mykiss; Sandblom and Axelsson, 2005), cardiac output is fully maintained. In other species, such as sea bass (Dicentrarchus labrax; Axelsson et al., 2002) and tilapia (Oreochromis hybrid sp.; Speers-Roesch et al., 2010), stroke volume does not compensate for the bradycardia, reducing cardiac output under hypoxia. Because these responses occur in conjunction with reduced arterial blood pressure (Sandblom and Axelsson, 2005; Speers-Roesch et al., 2010) it is hypothesized that their purpose is to reduce the cardiac power (see Glossary), and thus reduce O2 demand. Put simply, the acute hypoxia strategy of fish prioritizes reduced cardiac O2 demand as opposed to increased work to support uptake and delivery via perfusion.

During exercise, fishes prioritize increased O2 delivery to skeletal muscle through changes to blood flow (e.g. Kolok et al., 1993). To facilitate the increased skeletal muscle O2 demand, the heart rate will increase (tachycardia; see Glossary), as will stroke volume and cardiac output (reviewed by Farrell, 1991). In most fishes, an increase in stroke volume is more important than tachycardia – but this is species dependent. For example, yellowfin tuna (Thunnus albacares) exhibit a reduced stroke volume with exercise, yet cardiac output is still elevated because of substantial tachycardia (Korsmeyer et al., 1997). Exercise also has been shown to elevate arterial blood pressure (Stevens and Randall, 1967; Kiceniuk and Jones, 1977). Combined with elevated cardiac output, these changes work to substantially increase cardiac power, a critical limiting factor for maximal swim performance in fishes (e.g. Cox et al., 2017). O2 delivery is also a crucial determinant of cardiac power, which is most evident in fishes with coronary circulation (e.g. Ekström et al., 2018). Yet, coronary circulation is generally considered as an adaptation to an athletic lifestyle, and we are unaware of any suggestion of hypoxia-induced evolution of this trait in fishes. As such, it appears that the selective pressures of aerobic exercise and acute hypoxia on cardiac performance are fundamentally different in fishes, with exercise-adapted fish prioritizing increased O2 delivery and hypoxia-adapted fish prioritizing decreased O2 demand.

The second component of the Fick equation is the arteriovenous difference in total O2 content, which is a combination of and hemoglobin (Hb)–O2 (i.e. O2 bound to Hb). Hypoxia exposure and exercise both induce a number of similar physiological responses in the blood that protect total blood O2 content, including elevated hematocrit (reviewed by Gallaugher and Farrell, 1998) and the initiation of a catecholamine response to protect red blood cell intracellular pH (Primmett et al., 1986; Tetens and Christensen, 1987). The former raises the total blood O2-carrying capacity, whereas the latter protects Hb–O2 binding affinity during periods of systemic acidosis. But these similarities between the responses to hypoxia and exercise belie a number of important differences that can be the focus of selective pressure. The first notable difference is that although both hypoxia and exercise result in decreased blood , only hypoxia significantly reduces the total blood O2 content, at least with respect to the species studied to date (e.g. Holeton and Randall, 1967; Kiceniuk and Jones, 1977; Bushnell and Brill, 1992; Furimsky et al., 2003; McKenzie et al., 2004). The best datasets for illustrative purposes come from rainbow trout, where fish exercised at maximal swimming speed do not exhibit significantly reduced arterial total oxygen content (Brauner et al., 2000; McKenzie et al., 2004). Conversely, in response to hypoxia (4 kPa, 30 mmHg), the arterial blood of rainbow trout is significantly reduced to 37% saturation, as compared with ≥95% saturation under normoxia (Holeton and Randall, 1967). Differences between the responses to exercise and hypoxia also extend to venous blood, where evidence suggests that maximal exercise does not fully exhaust the available blood oxygen content, whereas hypoxia-exposed fish generally deplete venous oxygen reserves to maintain cardiac function. For example, the venous blood total O2 content of maximally exercised rainbow trout is ∼23% that of the arterial blood (Brauner et al., 2000). Conversely, exposure to a of 4 kPa – a value approximately 1.5 kPa above the reported Pcrit for rainbow trout (Svendsen et al., 2011) – lowers venous to 6 mmHg with only 3% Hb–O2 saturation (Holeton and Randall, 1967).

The data described above suggest that the O2-supply limitations that govern O2 uptake during exhaustive exercise (i.e. MMR) and O2 uptake at low ambient O2 levels (i.e. Pcrit) are fundamentally different in fishes. During exercise, increased cardiac output and hyperventilation (Stevens and Randall, 1967) maintain arterial blood O2 saturation and augment delivery to muscles, suggesting that aerobic constraints relate to O2-extraction efficiency, particularly in the heart. Conversely, hypoxia limitations are clearly governed by O2 uptake, which is benefited by hyperventilation (e.g. Ern and Esbaugh, 2016) in combination with high Hb–O2 binding affinity. This dichotomy is further supported by our understanding of the contribution of different Hb characteristics to O2 uptake and delivery. Several studies have highlighted the mechanistic link between high Hb–O2 affinity, whereby a low or reduced P50 (i.e. the O2 tension when Hb is 50% saturated with O2) improves aerobic performance in hypoxic environments (e.g. Mandic et al., 2009; Speers-Roesch et al., 2012; Pan et al., 2017). Conversely, recent data have highlighted an important role for the Root effect (see Glossary) in driving O2 extraction at the tissues when combined with plasma-accessible carbonic anhydrase activity (Rummer et al., 2013; Alderman et al., 2016; Harter et al., 2019), red blood cell Na+/H+ exchange (Rummer and Brauner, 2011) and cytoplasmic carbonic anhydrase activity (Dichiera and Esbaugh, 2020; Dichiera et al., 2020). This system has been specifically highlighted in the eye (Damsgaard et al., 2020), heart (Alderman et al., 2016) and red muscle (Rummer et al., 2013) of fishes, but has also been suggested to act to benefit systemic O2 delivery more broadly (Randall et al., 2014; Rummer and Brauner, 2015; Shu et al., 2018; Harter et al., 2019). Interestingly, an 8 day hypoxia acclimation significantly reduced the magnitude of the Root effect in red drum, while simultaneously improving Hb–O2 affinity. This further supports the notion of divergent evolutionary pressures exerted by hypoxia and exercise on fishes.

We would like to close this section by clarifying that we are not suggesting that exercise-based adaptations cannot benefit hypoxia tolerance, and vice versa. Elevated hematocrit, cardiac morphology and hyperventilatory responses are obvious examples that would benefit O2 supply capacity under any circumstance, and are known to respond positively to exercise and hypoxia acclimation in fishes (e.g. Yamamoto, 1987; Anttila et al., 2015). We fully support the notion that fish not specifically adapted to hypoxia will likely have a hypoxia tolerance that is a by-product of the selective pressures on MMR (Seibel and Deutsch, 2020). However, we suggest that hypoxia adaption can also include a suite of unique respiratory traits subject to selection, which may optimize αS at Pcrit to avoid an over-reliance on unsustainable anaerobic metabolism.

The effects of hypoxia on ɸ are specific to the supply (S) side of Eqn 1, which can be simplified for a reference body mass and temperature as . In those species where αS is not constant, there is a trend of gradually declining αS as the environment approaches normoxia (Fig. 2). The rate of change in αS is the determining factor in the accuracy of the ɸ estimate. To illustrate this, we have evaluated three different datasets as examples (Fig. 3). Red drum generally conform to the bisecting line model and have a Pcrit,max relatively close to normoxia (16.6 kPa; 79% air saturation). In this case, the estimated ɸ deviates from the measured values by <5%, and this only occurs near the Pcrit,max point. Common sole have a lower Pcrit,max and a more pronounced 26% deviation between measured and estimated ɸ values at 13.3 kPa. A more extreme example is shown for rock bass, which reveals a 51% overestimate of ɸ when compared with the measured value at 9 kPa. We would stress that the existence of a Pcrit,max below normoxia is not necessarily indicative of a species with an αS optimized for Pcrit, as evident in pumpkinseed (Fig. 2). However, Pcrit,max will represent the point of greatest deviation between estimated and measured ɸ in such fish species.

With these illustrative examples in mind, we have two recommendations for those applying the ɸ concept at an organismal level. The first is that a calculated Pcrit,max approximating normoxia (i.e. >80% air saturation) is suitable evidence that a species has a constant αS. The second recommendation is that when a Pcrit,max below 80% air saturation is observed (e.g. pumpkinseed), researchers should experimentally validate αS at the equivalent Pcrit,max oxygen tension. This will allow easy characterization of the consistency of αS, and quantify the maximum estimate error as a result of a non-linear αS.

A hyperbolic relationship between O2 supply capacity and is unlikely to directly impact the thermal sensitivity coefficients (E; see Glossary) of aerobic parameters, and the data of Lefrancois and Claireaux (2003) support this assumption. Their dataset measured MMR at multiple O2 tensions at three different temperatures, as well as SMR and Pcrit for those temperatures. Using these data, we calculated relatively similar values for thermal sensitivity of oxygen supply (ES) across the experimental range. Specifically, the ES values were 0.23 at Pcrit, 0.22 at 8 kPa, 0.23 at 13.3 kPa and 0.27 at 18.6 kPa (all values are equal to the mean of the reported measurement intervals).

A more important consideration with respect to warming was observed by Seibel and Deutsch (2020), who noted that the relative relationship between ES and the thermal sensitivity of oxygen demand (ED) may result in SMR exceeding MMR at very high temperatures, and more specifically that ES could not effectively predict MMR beyond a breakpoint that the authors designated as CTmax. This breakpoint is defined by the occurrence of a thermal plateau, or decline, in MMR that deviates from the exponential increase observed at lower temperatures. The authors used this relationship to suggest that impaired αS is not related to the decline in MMR because such an impairment would also be observed in Pcrit. This conclusion assumes that αS is constant at normoxic MMR and Pcrit, which as described above may not be true for a number of fish species. In fact, the available evidence suggests that αS limitations with warming in fishes are related to the ability to maintain cardiac output (Steinhausen et al., 2008; Eliason et al., 2011; Eliason et al., 2013), which, as described above, is not a major driver of Pcrit. It is important to note the practical implications of these findings with respect to predicting ɸ under warming conditions. The numerator of the ɸ formula is equivalent to MMR (e.g. ). This suggests that care should be taken when estimating ɸ at any temperature beyond which a thermally induced plateau in MMR is observed, as such extrapolation would result in an overestimate of ɸ.

As with the situation described above for hypoxia, the potential to overestimate ɸ is likely to affect only a subset of fishes. For example, species such as goldfish (Carassius auratus) (Fry and Hart, 1948), killifish (McBryan et al., 2013) and black sea bass (Centropristis striata) (Slesinger et al., 2019) all have documented thermal plateaus in MMR. Conversely, many species, such as Atlantic halibut (Hippoglossus hippoglossus) (Grans et al., 2014) and barramundi (Lates calcarifer) (Norin et al., 2014), show a consistent increase in MMR with warming. A thorough examination of the effects of warming on metabolic rate across a wide range of species can be found in Lefevre (2016). In the context of ɸ it is important that focus is placed on defining whether MMR collapses with warming, and identifying the temperature at which such breakpoints occur in species. To date, reduced cardiac performance has been highlighted as a likely cause for warming-induced collapses in MMR (e.g. Eliason et al., 2013); however, we should continue to explore additional causative factors that may contribute to this phenomenon. Intraspecies variation in such traits will ultimately be the focus of the selective processes that define the trajectory of species with climate change.

Thus far we have demonstrated that respiratory performance in fishes is not consistent with the assumption that αS is singularly evolved to meet the demands of exercise in all fishes. Instead, we hypothesize that the evolutionary pressures that have shaped respiratory performance in fishes can be divided into two categories. The first category contains those species adapted for exercise in their environment, which would be represented by a constant αS between Pcrit and Pcrit,max (e.g. red drum; Fig. 2C) (see Seibel and Deutsch, 2020). The second category contains those fishes whose αS is adapted to meet O2 demands at Pcrit, which is identifiable by declining αS as increases from Pcrit to a theoretical Pcrit,max (e.g. rock bass; Fig. 2H). It is important to recognize these patterns when studying the physiological mechanisms related to hypoxia tolerance and vulnerability in fishes. When αS is adapted for performance under normoxia, hypoxia vulnerability is likely to be a by-product of the selective pressures on MMR. Conversely, fishes with an αS that increases as O2 declines are likely to have specific adaptations to reduce hypoxia vulnerability.

Our second take home message is that a variable αS violates a central assumption of the metabolic index concept, and results in overestimated ɸ. The significance of such an error depends on the species, the scope of the error and how ɸ is used by researchers. For example, the recent work by Deutsch et al. (2020) used biogeographical and physiological data to predict the energetic limitations that constrain animal species distributions. Note that this work included a wide variety of marine animal phyla, and reported an average ɸcrit (i.e. the value of ɸ found at the equatorial or depth limit of a species distribution) of 3.3±0.3 (mean±s.e.m.; N=22) for marine fish species. For context, a subset of those species with both ɸcrit estimates and FAS data across a thermal range are shown in Fig. 4 (Table S2; data from Seibel and Deutsch, 2020; Ackerly and Esbaugh, 2021). Note that ɸcrit is an estimate of FAS, and that ɸcrit is quite high when compared with the FAS at the upper thermal range of laboratory studies. If we assume that the thermal ranges employed for the studies on FAS (Fig. 4A) are environmentally relevant, then the estimates of ɸcrit (Fig. 4B) suggest that the energetic limitations for many of these fishes equal the entirety of the theoretical AS. However, in cases where fish exhibit flexible αS across O2 tensions, or exhibit a thermally induced MMR collapse, the estimated ɸcrit is likely to be lower than reported.

An overestimated ɸcrit in a subset of fishes will have little bearing on the overall conclusions of Deutsch et al. (2020); namely, that the energetic limitations that define aquatic ectotherm species ranges are due to the combined effects of exercise, temperature and hypoxia. However, overestimates can change our understanding of the absolute energetic minimums that species experience, and how ɸ is used to predict the effects of climate change. In some ways, ɸcrit is an estimate of the buffer a species has against further warming and deoxygenation before they are forced to rely on anaerobic metabolism to meet their energetic demands. Species such as the black-axil chromis (ɸcrit=5.2) have a large buffer against respiratory stress, whereas Atlantic salmon (ɸcrit=2.2) have relatively little capacity for further O2 supply constraints. It is also important to recognize that species’ responses to climate change are complex, and survival may depend on poleward migration, phenotypic plasticity or other adaptations that allow species to maintain their existing ɸcrit. If we are to properly understand the role that ɸcrit may have in shaping biogeography and performance in fishes, it is important that we work with the best available estimates.

The metabolic index concept has placed a new and important significance on αS and the relationship between O2 consumption and , particularly at intermediate levels of hypoxia. In this Commentary, we reinforced the premise that this relationship can vary among species (Fry, 1947), and that many species show hyperbolic curves representative of an elevated αS as the animal approaches Pcrit. Although these findings have clear implications for the calculation of ɸ and ɸcrit, we would like to stress that this critique should not be viewed as a broad criticism of the metabolic index concept overall. We view any framework that can effectively predict the metabolic scope of a majority of aquatic ectotherms in response to environmental change as an incredibly powerful tool. But unifying theories are challenging, and inevitably there will be species that defy expectation. We argue that it is important to acknowledge such species and to develop alternative approaches that ensure a complete understanding of the effects of environmental change on animal performance. In particular, we hope this work places renewed focus on those species that may be adapted to hypoxic environments. This should include continued efforts to understand the physiological traits that define αS in these species, while also exploring the compounding effects of warming and deoxygenation on hypoxia vulnerability.

We would like to thank Brad Seibel for providing Excel spreadsheets that facilitated calculation of the thermal sensitivity of metabolic traits.

Funding

Funding for this Commentary was provided through a National Science Foundation grant to A.J.E. (#2002549), and a National Science Foundation Graduate Research Fellowship to B.N.J. (#1610403).

Ackerly
,
K. L.
and
Esbaugh
,
A. J.
(
2020
).
The additive effects of oil exposure and hypoxia on aerobic performance in red drum (Sciaenops ocellatus)
.
Sci. Total Environ.
737
,
140174
.
Ackerly
,
K. L.
and
Esbaugh
,
A. J.
(
2021
).
The effects of temperature on oil-induced respiratory impairment in red drum (Sciaenops ocellatus)
.
Aquat Toxicol.
233
,
105773
.
Agnisola
,
C.
,
McKenzie
,
D. J.
,
Pellegrino
,
D.
,
Bronzi
,
P.
,
Tota
,
B.
and
Taylor
,
E. W.
(
1999
).
Cardiovascular responses to hypoxia in the Adriatic sturgeon (Acipenser naccarii)
.
J. Appl. Ichthyol.
15
,
67
-
72
.
Alderman
,
S. L.
,
Harter
,
T. S.
,
Wilson
,
J. M.
,
Supuran
,
C. T.
,
Farrell
,
A. P.
and
Brauner
,
C. J.
(
2016
).
Evidence for a plasma-accessible carbonic anhydrase in the lumen of salmon heart that may enhance oxygen delivery to the myocardium
.
J. Exp. Biol.
219
,
719
-
724
.
Anttila
,
K.
,
Lewis
,
M.
,
Prokkola
,
J. M.
,
Kanerva
,
M.
,
Seppänen
,
E.
,
Kolari
,
I.
and
Nikinmaa
,
M.
(
2015
).
Warm acclimation and oxygen depletion induce species-specific responses in salmonids
.
J. Exp. Biol.
218
,
1471
-
1477
.
Axelsson
,
M.
,
Altimiras
,
J.
and
Claireaux
,
G.
(
2002
).
Post-prandial blood flow to the gastrointestinal tract is not compromised during hypoxia in the sea bass Dicentrarchus labrax
.
J. Exp. Biol.
205
,
2891
-
2896
.
Bozinovic
,
F.
and
Pörtner
,
H. O.
(
2015
).
Physiological ecology meets climate change
.
Ecol. Evol.
5
,
1025
-
1030
.
Brauner
,
C. J.
,
Thorarensen
,
H.
,
Gallaugher
,
P.
,
Farrell
,
A. P.
and
Randall
,
D. J.
(
2000
).
The interaction between O2 and CO2 exchange in rainbow trout during graded sustained exercise
.
Respir. Physiol.
119
,
83
-
96
.
Bushnell
,
P. G.
and
Brill
,
R. W.
(
1992
).
Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia
.
J. Comp. Physiol. B
162
,
131
-
143
.
Claireaux
,
G.
and
Chabot
,
D.
(
2016
).
Responses by fishes to environmental hypoxia: integration through Fry's concept of aerobic metabolic scope
.
J. Fish Biol.
88
,
232
-
251
.
Clark
,
T. D.
,
Sandblom
,
E.
and
Jutfelt
,
F.
(
2013
).
Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations
.
J. Exp. Biol.
216
,
2771
-
2782
.
Cox
,
G. K.
,
Crossley
,
D. A.
, II
,
Stieglitz
,
J. D.
,
Heuer
,
R. M.
,
Benetti
,
D. D.
and
Grosell
,
M.
(
2017
).
Oil exposure impairs In Situ cardiac function in response to β-adrenergic stimulation in cobia (Rachycentron canadum)
.
Environ. Sci. Technol.
51
,
14390
-
14396
.
Crans
,
K. D.
,
Pranckevicius
,
N. A.
and
Scott
,
G. R.
(
2015
).
Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)
.
J. Exp. Biol.
218
,
3264
-
3275
.
Damsgaard
,
C.
,
Lauridsen
,
H.
,
Harter
,
T. S.
,
Kwan
,
G. T.
,
Thomsen
,
J. S.
,
Funder
,
A. M. D.
,
Supuran
,
C. T.
,
Tresguerres
,
M.
,
Matthews
,
P. G. D.
and
Brauner
,
C. J.
(
2020
).
A novel acidification mechanism for greatly enhanced oxygen supply to the fish retina
.
eLife
9
,
e58995
.
Deutsch
,
C.
,
Ferrel
,
A.
,
Seibel
,
B.
,
Pörtner
,
H.-O.
and
Huey
,
R. B.
(
2015
).
Climate change tightens a metabolic constraint on marine habitats
.
Science
348
,
1132
-
1135
.
Deutsch
,
C.
,
Penn
,
J. L.
and
Seibel
,
B.
(
2020
).
Metabolic trait diversity shapes marine biogeography
.
Nature
585
,
557
-
562
.
Dichiera
,
A. M.
and
Esbaugh
,
A. J.
(
2020
).
Red blood cell carbonic anhydrase mediates oxygen delivery via the Root effect in red drum
.
J. Exp. Biol.
223
,
jeb232991
.
Dichiera
,
A. M.
,
McMillan
,
O. J. L.
,
Clifford
,
A. M.
,
Goss
,
G. G.
,
Brauner
,
C. J.
and
Esbaugh
,
A. J.
(
2020
).
The importance of a single amino acid substitution in reduced red blood cell carbonic anhydrase function of early-diverging fish
.
J. Comp. Physiol. B
190
,
287
-
296
.
Ekström
,
A.
,
Axelsson
,
M.
,
Gräns
,
A.
,
Brijs
,
J.
and
Sandblom
,
E.
(
2018
).
Importance of the coronary circulation for cardiac and metabolic performance in rainbow trout (Oncorhynchus mykiss)
.
Biol. Lett.
14
,
20180063
.
Eliason
,
E. J.
and
Farrell
,
A. P.
(
2016
).
Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet
.
J. Fish Biol.
88
,
359
-
388
.
Eliason
,
E. J.
,
Clark
,
T. D.
,
Hague
,
M. J.
,
Hanson
,
L. M.
,
Gallagher
,
Z. S.
,
Jeffries
,
K. M.
,
Gale
,
M. K.
,
Patterson
,
D. A.
,
Hinch
,
S. G.
and
Farrell
,
A. P.
(
2011
).
Differences in thermal tolerance among sockeye salmon populations
.
Science
332
,
109
-
112
.
Eliason
,
E. J.
,
Clark
,
T. D.
,
Hinch
,
S. G.
and
Farrell
,
A. P.
(
2013
).
Cardiorespiratory collapse at high temperature in swimming adult sockeye salmon
.
Conserv. Physiol.
1
,
cot008
.
Ern
,
R.
and
Esbaugh
,
A. J.
(
2016
).
Hyperventilation and blood acid-base balance in hypercapnia exposed red drum (Sciaenops ocellatus)
.
J. Comp. Physiol. B
186
,
447
-
460
.
Ern
,
R.
,
Norin
,
T.
,
Gamperl
,
A. K.
and
Esbaugh
,
A. J.
(
2016
).
Oxygen-dependence of upper thermal limits in fishes
.
J. Exp. Biol.
219
,
3376
-
3383
.
Ern
,
R.
,
Johansen
,
J. L.
,
Rummer
,
J. L.
and
Esbaugh
,
A. J.
(
2017
).
Effects of hypoxia and ocean acidification on the upper thermal niche boundaries of coral reef fishes
.
Biol. Lett.
13
,
20170135
.
Esbaugh
,
A. J.
(
2018
).
Physiological implications of ocean acidification for marine fish: emerging patterns and new insights
.
J. Comp. Physiol. B
188
,
1
-
13
.
Farrell
,
A. P.
(
1991
).
From hagfish to tuna: a perspective on cardiac function in fish
.
Physiol. Zool.
64
,
1137
-
1164
.
Farrell
,
A. P.
(
2007
).
Tribute to P. L. Lutz: a message from the heart – why hypoxic bradycardia in fishes?
J. Exp. Biol.
210
,
1715
-
1725
.
Farrell
,
A. P.
and
Richards
,
J. G.
(
2009
).
Chapter 11 defining hypoxia: an integrative synthesis of the responses of fish to hypoxia
. In
Fish Physiology
, Vol.
27
(
ed.
J.G.
Richards
,
A.P.
Farrell
and
C.J.
Brauner
), pp.
487
-
503
.
Academic Press
.
Farrell
,
A. P.
,
Eliason
,
E. J.
,
Sandblom
,
E.
and
Clark
,
T. D.
(
2009
).
Fish cardiorespiratory physiology in an era of climate change
.
Can. J. Zool.
87
,
835
-
851
.
Fry
,
F. E.
and
Hart
,
J. S.
(
1948
).
The relation of temperature to oxygen consumption in the goldfish
.
Biol. Bull.
94
,
66
-
77
.
Fry
,
F. E. J.
(
1947
).
Effects of the environment on animal activity
.
Ont. Fish. Res. Lab. Publication, Biol. Ser.
55
,
1
-
62
.
Furimsky
,
M.
,
Cooke
,
S. J.
,
Suski
,
C. D.
,
Wang
,
Y.
and
Tufts
,
B. L.
(
2003
).
Respiratory and Circulatory Responses to Hypoxia in Largemouth Bass and Smallmouth Bass: Implications for “Live-Release” Angling Tournaments
.
Trans. Am. Fish. Soc.
132
,
1065
-
1075
.
Gallaugher
,
P.
and
Farrell
,
A. P.
(
1998
).
Hematocrit and blood oxygen-carrying capacity
. In
Fish Physiology
, Vol.
17
.
Fish Respiration
(ed.
S. F.
Perry
and
B. L.
Tufts
), pp.
185
-
227
.
Academic Press
.
Gamperl
,
A. K.
and
Driedzic
,
W. R.
(
2009
).
Chapter 7 Cardiovascular Function and Cardiac Metabolism
. In
Fish Physiology
, Vol.
27
(
eds.
A.P.F.
Jeffrey
,
G.
Richards
and
J.B.
Colin
), pp.
301
-
360
.
Academic Press
.
Grans
,
A.
,
Jutfelt
,
F.
,
Sandblom
,
E.
,
Jonsson
,
E.
,
Wiklander
,
K.
,
Seth
,
H.
,
Olsson
,
C.
,
Dupont
,
S.
,
Ortega- Martinez
,
O.
,
Einarsdottir
,
I.
et al. 
(
2014
).
Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut
.
J. Exp. Biol.
217
,
711
-
717
.
Harter
,
T. S.
,
Zanuzzo
,
F. S.
,
Supuran
,
C. T.
,
Gamperl
,
A. K.
,
Brauner
,
C. J.
(
2019
).
Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish
.
Proc. Biol. Sci.
286
,
20190339
.
Holeton
,
G. F.
and
Randall
,
D. J.
(
1967
).
The effect of hypoxia upon the partial pressure of gases in the blood and water afferent and efferent to the gills of rainbow trout
.
J. Exp. Biol.
46
,
317
-
327
.
Jutfelt
,
F.
,
Norin
,
T.
,
Ern
,
R.
,
Overgaard
,
J.
,
Wang
,
T.
,
McKenzie
,
D. J.
,
Lefevre
,
S.
,
Nilsson
,
G. E.
,
Metcalfe
,
N. B.
,
Hickey
,
A. J. R.
et al. 
(
2018
).
Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology
.
J. Exp. Biol.
221
,
jeb169615
.
Keeling
,
R. E.
,
Körtzinger
,
A.
and
Gruber
,
N.
(
2010
).
Ocean deoxygenation in a warming world
.
Ann. Rev. Mar. Sci.
2
,
199
-
229
.
Kiceniuk
,
J. W.
and
Jones
,
D. R.
(
1977
).
The oxygen transport system in trout (Salmo gairdneri) during sustained exercise
.
J. Exp. Biol.
69
,
247
-
260
.
Kolok
,
A. S.
,
Spooner
,
M. R.
and
Farrell
,
A. P.
(
1993
).
The effect of exercise on the cardiac output and blood flow distribution of the largescale sucker catostomus macrocheilus
.
J. Exp. Biol.
183
,
301
-
321
.
Korsmeyer
,
K. E.
,
Lai
,
N. C.
,
Shadwick
,
R. E.
and
Graham
,
J. B.
(
1997
).
Heart rate and stroke volume contribution to cardiac output in swimming yellowfin tuna: response to exercise and temperature
.
J. Exp. Biol.
200
,
1975
-
1986
.
Lefevre
,
S.
(
2016
).
Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction
.
Conser. Physiol.
4
,
cow009
-
cow009
.
Lefrançois
,
C.
and
Claireaux
,
G.
(
2003
).
Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole Solea solea
.
Mar. Ecol. Prog. Ser.
259
,
273
-
284
.
Mandic
,
M.
,
Todgham
,
A. E.
and
Richards
,
J. G.
(
2009
).
Mechanisms and evolution of hypoxia tolerance in fish
.
Proc. Biol. Sci.
276
,
735
-
744
.
McBryan
,
T. L.
,
Anttila
,
K.
,
Healy
,
T. M.
and
Schulte
,
P. M.
(
2013
).
Responses to temperature and hypoxia as interacting stressors in fish: implications for adaptation to environmental change
.
Integr. Comp. Biol.
53
,
648
-
659
.
McKenzie
,
D. J.
,
Wong
,
S.
,
Randall
,
D. J.
,
Egginton
,
S.
,
Taylor
,
E. W.
and
Farrell
,
A. P.
(
2004
).
The effects of sustained exercise and hypoxia upon oxygen tensions in the red muscle of rainbow trout
.
J. Exp. Biol.
207
,
3629
-
3637
.
McKenzie
,
D. J.
,
Skov
,
P. V.
,
Taylor
,
E. W.
,
Wang
,
T.
and
Steffensen
,
J. F.
(
2009
).
Abolition of reflex bradycardia by cardiac vagotomy has no effect on the regulation of oxygen uptake by Atlantic cod in progressive hypoxia
.
Comp. Biochem. Physiol. A. Mol. Integr. Physiol.
153
,
332
-
338
.
Negrete
,
B.
Jr.
and
Esbaugh
,
A. J.
(
2019
).
A methodological evaluation of the determination of critical oxygen threshold in an estuarine teleost
.
Biol. Open
8
,
bio045310
.
Nelson
,
J. S.
,
Grande
,
T. C.
and
Wilson
,
M. V. H.
(
2016
).
Fishes of the World
, 5th edn.
Hoboken, New Jersey
,
USA
:
John Wiley & Sons
.
Norin
,
T.
and
Clark
,
T. D.
(
2016
).
Measurement and relevance of maximum metabolic rate in fishes
.
J. Fish Biol.
88
,
122
-
151
.
Norin
,
T.
,
Malte
,
H.
and
Clark
,
T. D.
(
2014
).
Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures
.
J. Exp. Biol.
217
,
244
-
251
.
Pan
,
Y. K.
,
Ern
,
R.
,
Morrison
,
P. R.
,
Brauner
,
C. J.
and
Esbaugh
,
A. J.
(
2017
).
Acclimation to prolonged hypoxia alters hemoglobin isoform expression and increases hemoglobin oxygen affinity and aerobic performance in a marine fish
.
Sci. Rep.
7
,
7834
.
Petersen
,
L. H.
and
Gamperl
,
A. K.
(
2011
).
Cod (Gadus morhua) cardiorespiratory physiology and hypoxia tolerance following acclimation to low-oxygen conditions
.
Physiol. Biochem. Zool.
84
,
18
-
31
.
Pörtner
,
H. O.
(
2010
).
Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems
.
J. Exp. Biol.
213
,
881
-
893
.
Pörtner
,
H. O.
and
Farrell
,
A. P.
(
2008
).
Physiology and climate change
.
Science
322
,
690
-
692
.
Portner
,
H. O.
and
Knust
,
R.
(
2007
).
Climate change affects marine fishes through the oxygen limitation of thermal tolerance
.
Science
315
,
95
-
97
.
Primmett
,
D. R.
,
Randall
,
D. J.
,
Mazeaud
,
M.
and
Boutilier
,
R. G.
(
1986
).
The role of catecholamines in erythrocyte pH regulation and oxygen transport in rainbow trout (Salmo gairdneri) during exercise
.
J. Exp. Biol.
122
,
139
-
148
.
Randall
,
D. J.
,
Rummer
,
J. L.
,
Wilson
,
J. M.
,
Wang
,
S.
and
Brauner
,
C. J.
(
2014
).
A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes
.
J. Exp. Biol.
217
,
1205
-
1214
.
Ravi
,
V.
and
Venkatesh
,
B.
(
2008
).
Rapidly evolving fish genomes and teleost diversity
.
Curr. Opin. Genet. Dev.
18
,
544
-
550
.
Richards
,
J. G.
(
2011
).
Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia
.
J. Exp. Biol.
214
,
191
-
199
.
Rummer
,
J. L.
and
Brauner
,
C. J.
(
2011
).
Plasma-accessible carbonic anhydrase at the tissue of a teleost fish may greatly enhance oxygen delivery: in vitro evidence in rainbow trout, Oncorhynchus mykiss
.
J. Exp. Biol.
214
,
2319
-
2328
.
Rummer
,
J. L.
and
Brauner
,
C. J.
(
2015
).
Root effect haemoglobins in fish may greatly enhance general oxygen delivery relative to other vertebrates
.
PLoS ONE
10
,
e0139477
.
Rummer
,
J. L.
,
McKenzie
,
D. J.
,
Innocenti
,
A.
,
Supuran
,
C. T.
and
Brauner
,
C. J.
(
2013
).
Root effect hemoglobin may have evolved to enhance general tissue oxygen delivery
.
Science
340
,
1327
-
1329
.
Sandblom
,
E.
and
Axelsson
,
M.
(
2005
).
Effects of hypoxia on the venous circulation in rainbow trout (Oncorhynchus mykiss)
.
Comp. Biochem. Physiol. A. Mol. Integr. Physiol.
140
,
233
-
239
.
Seibel
,
B. A.
and
Deutsch
,
C.
(
2020
).
Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature
.
J. Exp. Biol.
223
,
jeb210492
.
Shu
,
J. J.
,
Harter
,
T. S.
,
Morrison
,
P. R.
and
Brauner
,
C. J.
(
2018
).
Enhanced hemoglobin-oxygen unloading in migratory salmonids
.
J. Comp. Physiol. B
188
,
409
-
419
.
Slesinger
,
E.
,
Andres
,
A.
,
Young
,
R.
,
Seibel
,
B.
,
Saba
,
V.
,
Phelan
,
B.
,
Rosendale
,
J.
,
Wieczorek
,
D.
and
Saba
,
G.
(
2019
).
The effect of ocean warming on black sea bass (Centropristis striata) aerobic scope and hypoxia tolerance
.
PLOS ONE
14
,
e0218390
.
Speers-Roesch
,
B.
,
Sandblom
,
E.
,
Lau
,
G. Y.
,
Farrell
,
A. P.
and
Richards
,
J. G.
(
2010
).
Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia
.
Am. J. Physiol. Regul. Integr. Comp. Physiol.
298
,
R104
-
R119
.
Speers-Roesch
,
B.
,
Richards
,
J. G.
,
Brauner
,
C. J.
,
Farrell
,
A. P.
,
Hickey
,
A. J.
,
Wang
,
Y. S.
and
Renshaw
,
G. M.
(
2012
).
Hypoxia tolerance in elasmobranchs. I. Critical oxygen tension as a measure of blood oxygen transport during hypoxia exposure
.
J. Exp. Biol.
215
,
93
-
102
.
Steinhausen
,
M. F.
,
Sandblom
,
E.
,
Eliason
,
E. J.
,
Verhille
,
C.
and
Farrell
,
A. P.
(
2008
).
The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka)
.
J. Exp. Biol.
211
,
3915
-
3926
.
Stevens
,
E. D.
and
Randall
,
D. J.
(
1967
).
Changes in blood pressure, heart rate and breathing rate during moderate swimming activity in rainbow trout
.
J. Exp. Biol.
46
,
307
-
315
.
Svendsen
,
J. C.
,
Steffensen
,
J. F.
,
Aarestrup
,
K.
,
Frisk
,
M.
,
Etzerodt
,
A.
and
Jyde
,
M.
(
2011
).
Excess posthypoxic oxygen consumption in rainbow trout (Oncorhynchus mykiss): recovery in normoxia and hypoxia
.
Can. J. Zool.
90
,
1
-
11
.
Tetens
,
V.
and
Christensen
,
N. J.
(
1987
).
Beta-adrenergic control of blood oxygen affinity in acutely hypoxia exposed rainbow trout
.
J. Comp. Physiol. B
157
,
667
-
675
.
Wood
,
C. M.
(
2018
).
The fallacy of the Pcrit – are there more useful alternatives?
J. Exp. Biol.
221
,
jeb163717
.
Yamamoto
,
K.-I.
(
1987
).
Contraction of spleen in exercised cyprinid
.
Comp. Biochem. Physiol. A Comp. Physiol.
87
,
1083
-
1087
.

Competing interests

The authors declare no competing or financial interests.

Supplementary information