‘Nothing in biology makes sense except in the light of evolution’ is a much cited message from a paper by Dobzhansky (Dobzhansky, 1973). It emphasizes that identifying the principles, similarities and differences of structures and functions between organisms, their families, phyla and domains leads to an understanding of the pathways of evolution. Of course, biology encompasses experimental animal biology, which includes the comparative study of functions within or across phyla to identify the principles maintained and their potential and special modifications. Knowledge of unifying functional principles provides the foundation when addressing the sensitivities of species to environmental change, considering their phylogeny and mode of life. As experimental biology presently aims at becoming involved in conservation science, one question also is how to shape research to obtain the most powerful contributions to this field.
In this context, the recent paper by Clark and colleagues (Clark et al., 2013) discusses high quality measurements of respiratory rates in fishes but does not fully appreciate the ecological and evolutionary framework within which relevant concepts have been developed and applied. The text by Clark et al. is suggestive that the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis [including aerobic scope, see parallel Correspondence by Anthony Farrell in this issue (Farrell, 2013)] as well as associated constraints may only work in some but not all fish species. Does this mean that for other species (to be identified), OCLTT needs to be replaced with alternative concepts? Are there any? Here, the authors may have overlooked the fact that OCLTT addresses a unifying ecological and evolutionary principle in (aquatic) animals: the specialization on temperature and the first lines of thermal limitation are set at the highest level of biological organization, and involve oxygen supply systems and their capacities in relation to oxygen demand. Such constraints have been identified in representative species from key animal phyla and one wonders whether (and how) individual species can be exempt from such principle? A conceivable way out might be through a secondary reduction of environmental constraints or through exceptional evolutionary adaptations. Following OCLTT principles, the movement of species into highly oxygenated environments such as air might have triggered the alleviation of such constraints. Such evidence is in fact emerging for the recurrent evolution of breathing air in crustaceans and fishes (F.G., M. Fusi, A. Barausse, B. Mostert, H.-O.P. and S. Cannicci, unpublished results). In cold polar oceans, oxygen availability in excess of demand may also have led to the relaxation of oxygen constraints and to losses of associated functions as discussed for polar fishes (Pörtner et al., 2013). Exceptional adaptations may exist in insects due to the use of tracheal rather than convective oxygen supply systems. Interestingly, OCLTT principles apply to insect aquatic larvae (Verberk and Bilton, 2011), leading to relevant perspectives concerning insect evolution. So Clark and colleagues have missed out on the question of what OCLTT can contribute to addressing the role of oxygen and capacity limitations as early constraints in animal evolution in the aquatic realm.
Unifying physiological principles find validation in an ecological context, for a specific life stage, season or in a biogeographical context. Field studies provide evidence that OCLTT sets southern distribution limits in European eelpout (Pörtner and Knust, 2007) or is the key constraint during a critical life cycle period such as the spawning migration of Pacific salmon (Farrell et al., 2008). In both cases, species operate at the limits of their warm acclimatization capacity. These examples also make clear that animals do not continuously exploit the functional capacity associated with OCLTT and do not experience the respective limitations everywhere in their natural range. However, OCLTT defines not only thermal specialization of species and their performance breadths but also the potential to allocate aerobic energy and associated functional tradeoffs. Aerobic scopes for exercise, growth or reproduction are high level proxies for this potential, with the suitability of a proxy depending on the lifestyle and lifestage of a species. Such proxy should be determined in a stress-free situation. Enforced studies of excess post-exercise oxygen consumption (EPOC) are clearly not suitable to measure the subtleties of oxygen and energy allocation in the sense of OCLTT. If EPOC studies are used nonetheless to determine thermal limits, the data need to be tested against ecological realities. In this context, Clark et al. seem to misinterpret the OCLTT concept: it does not assume optimum and preferred temperatures of a species to be similar. Several examples of a mismatch between optimal and preferred temperature are known for fish (Angiletta, 2009).
The unfounded criticism of the OCLTT concept comes with the request that more and more individual species (of fishes) should be studied to see whether it works or not in each individual case. In an evolutionary context, a relevant approach would rather be to ask what the concept can do for understanding differences between species with respect to performance, specific lifestyle, thermal limitations and underlying mechanisms. OCLTT links levels of biological organization and places apparently disconnected mechanisms into a larger context. OCLTT casts new light on the differential energy costs of various processes and their role in thermal limitation, for example the cost of oxygen supply depending on oxygen availability (Mark et al., 2002) or depending on the functioning of blood pigments (Giomi and Pörtner, 2013). Furthermore, the OCLTT framework contributes to an integrated view of climate-related stressors, their role in evolutionary crises in Earth history, and their functional consequences for animal evolution (Pörtner et al., 2005; Knoll et al., 2007; Clarke and Pörtner, 2010). Unfortunately, apart from their criticism of OCLTT and the present uses of aerobic scope, Clark and colleagues do not even attempt to suggest alternative concepts that would be equally relevant in ecology and evolutionary biology and equally suitable to explain the shape and position of performance curves on the temperature scale.
Stepping back from the present debate, we should put an evolutionary time scale on what experimental findings mean for each species or group in its ecological situation. Such wider context always requires consideration when elaborating what is unifying and what has become specific for the species studied. Finally, in light of climate change it is urgent that we develop a consensus on a concept representing climate-related physiology, for a solid cause and effect understanding and to convincingly voice the contributions of the experimental community. If existing concepts are not convincing enough then alternative ones should be proposed or present ones should be developed further, especially those backed by strong evidence across phyla such as OCLTT. It seems more promising to fill the existing framework than to reinvestigate the wheel for each animal species.
