The Commentary by Pörtner, Bock and Mark (Pörtner et al., 2017) elaborates on the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Journal of Experimental Biology Commentaries allow for personal and controversial views, yet the journal also mandates that ‘opinion and fact must be clearly distinguishable’ (http://jeb.biologists.org/content/article-types#comms). We contend that Pörtner et al. (2017) do not meet this requirement, and that they present a biased account of the OCLTT hypothesis. We raise two main points: (1) Pörtner et al. (2017) do not do justice to the growing number of empirical studies that failed to support the OCLTT hypothesis when specifically testing its predictions, and (2) in response to these studies, and without new empirical evidence to support OCLTT, Pörtner and colleagues have gradually redefined the core assumptions of the hypothesis so that it is increasingly difficult to test and has lost predictive power.
Overlooking evidence against the hypothesis
Pörtner et al. (2017) portray the OCLTT hypothesis as a widely accepted consensus theory with great predictive power and depth. This impression is created by selective sampling of the literature (Pörtner is an author of 46 of the 98 references in Pörtner et al., 2017), and failure to acknowledge and incorporate studies that do not support the OCLTT hypothesis. In reality, the ecophysiological community is divided over the validity and utility of the hypothesis.
The controversy mainly revolves around whether OCLTT mechanisms are prevalent across ectotherms during warming, especially in response to long-term climate change. We agree that tissue oxygen limitation has been reported in some species during acute thermal challenges, and that oxygen limitation may be the direct cause of deterioration in whole-animal performance in some animals in some contexts. However, a multitude of studies not cited in Pörtner et al. (2017) do not support oxygen limitation as the main factor limiting performance at high temperatures in ectotherms, emphasising that the OCLTT hypothesis is far from universally accepted (see discussions and references in Clark et al., 2013a,b; Jutfelt et al., 2014; Lefevre, 2016; Schulte, 2015).
There are a number of problems associated with the OCLTT hypothesis, including the points in Box 1 and the following findings. For marine ectotherms, a meta-analysis of aerobic metabolic rates failed to find a clear optimal temperature for aerobic scope in the majority of species during acute and long-term thermal exposures (Lefevre, 2016), contradicting a foundational assumption of the OCLTT hypothesis. In fish, the thermal profiles of aerobic scope and cardiac performance (following acute and long-term exposures) often do not align with ecologically relevant temperatures encountered by the species, and do not match the profiles of other important performances such as growth and reproduction (e.g. Gräns et al., 2014; Norin et al., 2014). Manipulations of ambient oxygen levels usually fail to alter acute thermal tolerance until severe hypoxia is reached (Brijs et al., 2015; Ern et al., 2016; Verberk et al., 2016), and altered tissue oxygenation capacity and aerobic scope generally have little effect on acute thermal tolerance (Brijs et al., 2015; Ekström et al., 2016; Wang et al., 2014). In arthropods, a review of the scientific literature demonstrated that oxygen limitation during acute warming is not universal but instead is restricted to certain groups (Verberk et al., 2016).
Low testability of many claims means that unequivocal evidence for OCLTT mechanisms is lacking and confidence should be withheld.
Vague terminology and poorly defined concepts make measurements of these parameters prone to biased interpretations (e.g. pejus temperature, aerobic power budget).
Continuously changing y-axis labels on the famous bell-shaped thermal profiles (Fry curve or aerobic scope curve). In Pörtner et al. (2017) they read: ‘Aerobic window (steady state)’ in box 1 and ‘Steady-state routine performance levels (—) at different metabolic rates (e.g. —)’ in box 2, and the text refers to ‘aerobic power budget’ (Pörtner et al., 2017).
High reliance on schematic (aspirational) diagrams rather than empirically derived data to support the OCLTT hypothesis (e.g. see fig. 2 in Pörtner et al., 2017).
Although the OCLTT hypothesis is presented as mechanistic in Pörtner et al. (2017), most of the evidence supporting the hypothesis is indirect and derived from correlations among processes (i.e. negating the ability to attribute cause and effect).
The claim that tissue hypoxia is the first and most important cause of the downstream effects during warming (effects on growth, reproduction, foraging, immune competence, behaviours and competitiveness) has been asserted, not demonstrated.
Incorrectly considering aerobic scope or oxygen delivery capacity as the ‘energy’ available to animals, when in fact it is only a permissive factor compared with other constraints (e.g. food availability).
Overreaching conclusions and bold climate change-related extrapolations of results from acute, non-steady-state thermal challenges.
It is concerning that Pörtner et al. (2017) argue that studies using acute thermal challenges and ‘non-steady-state’ experiments are unsuitable for testing the OCLTT hypothesis, despite these authors using the same acute and non-steady-state approaches to initially devise the hypothesis and to continue to support their assertions. Results from studies based on acute and chronic thermal and hypoxic challenges that have failed to support the OCLTT hypothesis are of no lesser value than those claiming to support the hypothesis. If Pörtner et al. (2017) wish to develop the OCLTT hypothesis in accordance with available evidence, these critical studies should not be misrepresented, dismissed or ignored, but instead they should be weighed equally as those favouring the hypothesis.
The changing nature of the hypothesis
We are concerned with the way the OCLTT hypothesis continues to morph, despite the absence of new supportive data. Pörtner et al. (2017) modify the hypothesis compared with the many previous reviews of the subject, from the original focus on maximum metabolism and aerobic scope to a new emphasis on routine metabolic rates. While the relevance of the OCLTT hypothesis in a long-term ecologically relevant context remains unresolved, the added reservations for the ‘aerobic power budget’ and ‘functional reserves’ make the hypothesis much less testable. Indeed, oxygen limitation is readily testable at maximum physiological function (e.g. maximum oxygen uptake rate, or critical thermal maximum), yet it is difficult to investigate the existence or avoidance of local tissue oxygen limitation during routine activity. Moreover, the concept that oxygen might be limiting at routine levels of activity seems illogical; it is hard to imagine why animals would allow tissue hypoxia to become severe enough to inflict performance declines at moderate levels of activity when possessing the functional capacity to significantly increase oxygen delivery to tissues. That assertion in Pörtner et al. (2017) is possibly untestable with available techniques and technologies.
To conclude, counter to the impression given in Pörtner et al. (2017), there is no consensus in the field on the generality of OCLTT mechanisms. While there is empirical support for the OCLTT hypothesis in certain contexts, there are substantial datasets contradicting predictions derived from the hypothesis. Moreover, the theoretical basis of the hypothesis appears to have shifted markedly. We encourage Pörtner and colleagues to consider all tests of the predictions originally made by the OCLTT hypothesis, and to provide a balanced assessment of these tests to draw conclusions about its generality. It is crucial that the OCLTT hypothesis retains clear and testable predictions, so that empirical scientists can evaluate in which animals and contexts the hypothesis might have predictive value. We would appreciate a clear guide on the experimental approaches deemed satisfactory for testing the current OCLTT hypothesis, and we welcome an open collaboration to conduct this research.
