Science is built on skepticism. We therefore appreciate the high interest in our paper (Pörtner et al., 2017) and welcome a debate that has been going on for some time. Our commentary started as a draft correspondence with specific criticism of a paper, and was then invited by the journal editor to address misunderstandings about the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Here we express some general concerns and the need to widen the debate as well as to eliminate an overly normative tone.
Further debate needs to be based on an interdisciplinary effort towards bridging the historic disciplinary divide between physiology and ecology. At present, this most needed connection is prevented by a gap between many experimental findings and ecological reality. We assume, however, that agreement exists on the need to better understand the molecular, biochemical, physiological and anatomical factors that shape biogeographic distributions, abundance and biodiversity of ectotherms. Comparative physiology needs to meet this challenge in order to contribute to predictions of climate-related responses at the local community to ecosystem levels. Failure to embed physiological studies in a wider context can lead to the marginalization of experimental one-species studies as ‘simplistic’ (Boero et al., 2004), whereby the physiological (functional) background is left out in explaining ecological patterns and theory (Killen et al., 2014) owing to lack of realism (Boyd et al., 2017). This also applies if the approach is not sufficiently comprehensive, e.g. if constrained to molecular markers or behavioral change. Physiology needs to contribute to explaining demographic and vital rates, movement and shifts in species interactions – across multiple scales.
This challenge exposes classical physiological testing to scrutiny. In brief, fitting physiological patterns to related field phenomena using the OCLTT hypothesis has emphasized the relevance of (1) routine (i.e. sustainable) performance and (2) subtle functional constraints at their onset, as well as the physiological and molecular indicators of those constraints and, only then, (3) time-dependent tolerance to extreme challenges such as heat waves as captured by critical temperature of OCLTT and critical thermal maximum (CTmax) (Pörtner et al., 2017). Importantly, investigations of these three factors need to precisely consider the species-specific ecological background. Furthermore, the temperature-dependent long-term performance window is mirrored in relevant gene expression patterns (e.g. Windisch et al., 2014). We have assessed several papers identified as candidates for alternate evidence and found that some approaches used do not meet relevant requirements (Pörtner et al., 2017). For example, we caution against testing the role of oxygen in OCLTT using CTmax (too insensitive) and with an inward look into classic physiological knowledge. Insofar, we argue that many of these studies were at high risk to fail and indeed, we interpret many of their findings differently. This is a natural process of scientific debate, which will ultimately push the field forwards.
Importantly, and often miscommunicated, the OCLTT hypothesis reaches beyond aerobic scope for exercise (AS) to include various routine performances fueled by the more comprehensive aerobic power budget. As a result of trade-offs within the total energy budget, individual physiological processes such as growth and exercise may or may not have different thermal optima. The OCLTT concept takes into account the fact that subtle physiological constraints at the onset of thermal limitation are already connected to ecological change. Pejus temperatures (Tp) indicate the onset of limitation and are most relevant on ecological terms in sensitive life stages, also seen in an air breather (e.g. Smith et al., 2015), and during routine activity.
The methods used to develop the OCLTT hypothesis are all available and provide relevant data with new avenues for their interpretation. The challenging of conventional methods implies that more sophisticated methods and indicators may need to be developed (as for an insect study, Teague et al., 2017). Importantly, to connect closely to ecological change, studies need to consider the long-term consequences of subtle functional constraints for performance capacity and competitive strength in an experimental setting that would not hurt the ecological context for the respective life stage (e.g. salmon migration, Farrell, 2016). Indeed, such requirements are rarely met in purely physiological studies. Pushing the OCLTT hypothesis back to early stages of the concept does not support further progress. The request for a detailed guide on how to investigate OCLTT is unusual as our studies of different levels of biological organization and field phenomena are repeatable and thereby, in addition to supporting our conclusions, fulfil relevant requirements associated with scientific publishing. That said, jointly developing a best practice guide would, in fact, be rewarding.
The OCLTT hypothesis also strives to integrate levels of biological organization from gene to cell and organism to ecosystem. As no alternative integrative concept is presently available, we anticipate that the OCLTT hypothesis will continue to evolve and be useful for those working in an ecological context as closely as we are trying to do. We also reiterate that the OCLTT concept considers the evolutionary context, beyond the testing of as many individual species as possible (ibid). We need to understand the constraints and changes that have affected key physiological functions over evolutionary time. ‘Stamp collecting’ many species at an adult stage does not help here, if the ecology and life history of each species as well as temperature-induced constraints on critical life stages are not considered in the interpretation (e.g. Marcus and Boero, 1998; Farrell, 2016; Boardman and Terblanche, 2015; Pörtner et al., 2017). In light of the need to carefully match hypotheses and data, one wonders whether the database of the careful meta-analysis referred to can provide evidence for or against OCLTT.
Finally, we thank Jutfelt et al. for the offer of collaboration, which we happily accept. At the same time, we encourage everybody to develop alternative concepts equally powerful in bridging the gap between physiology and ecology that we can then test together. We need a healthy competition of concepts with a perspective to build linkages to other disciplines rather than an inward-looking overly narrow normative debate, which, if successful, would constrain future inter- and transdisciplinary research. We might then also miss a chance to enhance the contribution of experimental biology to addressing questions of high societal relevance, such as the impacts of climate change (e.g. Urban et al., 2011; Pörtner et al., 2014; Poloczanska et al., 2014). In light of the difference of opinion regarding the applicability of the OCLTT hypothesis, perhaps now is the time to move the debate to a more flexible forum than journal correspondence, which is restrictive in its length and therefore its scope.
We thank A. P. Farrell and L. S. Peck for supportive discussions. Diverse support for the OCLTT hypothesis and the need for a closer link between ecological and physiological patterns was expressed by various national and international colleagues whom we contacted during the preparation of this reply. Among others this includes A. Bates, M. Burrows, G. Claireaux, M. J. Costello, G. Lannig, B. Michaelidis, J. García Molinos, E. Poloczanska, D. Schoeman, I. Sokolova, D. Storch and H. Windisch, some of whom also provided additional comments, which were gratefully incorporated.