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Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature

Brad A. Seibel, Curtis Deutsch

Preprint posted on July 14, 2019 https://www.biorxiv.org/content/10.1101/701417v1

Do body size and temperature affect the ability to supply oxygen? This preprint analyses the evolution of oxygen supply capacity across a wide range of species.

Selected by Charlotte Nelson

Context

Environmental oxygen availability is classically held as the limiting factor in metabolic rate and aerobic scope (the difference between the maximum and minimum amounts of oxygen that an animal consumes) which is thought to constrain body size and thermal tolerance. When plotted against temperature, the peak in aerobic scope is often believed to represent a species’ thermal optimum – the temperature to which they are best adapted – however various studies have suggested that this does not actually represent the thermal environment which an animal may naturally be found. Selection for maximum metabolic rate is also likely an important driver of endothermy in vertebrates and the ability to supply oxygen is clearly critically linked to this. This study aimed to assess the hypothesis that oxygen transport systems have evolved to meet the maximal oxygen demand at today’s current, high oxygen partial pressure. The physiological ability to supply oxygen was calculated for 47 species with widespread evolutionary and life histories.

 

Key Findings and Relevance

The authors found that regardless of body mass or temperature, the capacity to supply oxygen is tightly matched to the maximum evolved demand at the highest reliably available oxygen pressure experienced by the species. For most species studied, this maximum oxygen availability is represented by the current atmospheric pressures. Therefore, reductions in atmospheric oxygen availability, as are thought to become more common in aquatic environments under predicted climate change scenarios, would result in decreases in maximum metabolic performance.

However, and contrary to the accepted school of thought, the observable decrease in performance at high temperatures was not a result of an inability to provide sufficient oxygen, but instead due to inefficiency of the metabolic machinery to utilize oxygen. Similarly, this data suggests that metabolic scaling and temperature-induced reductions in body size are not the result of a size-related oxygen supply limitation as is suggested by other theories (metabolic theory of ecology, gill oxygen limitation theory) because the oxygen supply capacity evolves to meet increasing demand at larger sizes. This suggests a strong selective pressure acting on the oxygen supply system to meet the maximal oxygen demand; a scenario which is enhanced for those species living in hypoxic environments.

The authors contend that species do not evolve excess capacity to provide oxygen or an excess capacity for its utilization, and that a species’ critical oxygen pressure reflects adaptations in aerobic scope, rather than representing an indicator of hypoxia tolerance. These findings are in line with the established theory of symmorphosis; the concept in which each step of a process has evolved in concert, without a rate limiting step and suggests that organisms do not possess excess capacity for oxygen supply or usage.

This study provides a novel standpoint in the debate surrounding the evolution of thermal tolerance, body mass scaling and oxygen supply limitation. This simple relationship may alter the way we think about various important physiological concepts and their ecological interpretation.

 

Open questions

  • How do species that are known as ‘living fossils’ fit into this framework? Does this relationship still hold for archaic species which have changed little in recent history?
  • How do characteristics such as the Root effect observed in teleost hemoglobins play into this relationship?
  • How can this new relationship help to inform how species may react to global climate change, and can we use it to mitigate effects or manage populations more successfully?
  • If oxygen supply capacity has evolved to match oxygen availability, then why is CTmax generally higher than any temperature experienced by an animal?

 

References

Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. and West, G. B. (2004). Towards a Metabolic Theory of Ecology. Ecology 85, 1771-1789.

Cheung, W. W. L., Sarmiento, J. L., Dunne, J., Frölicher, T. L., Lam, V. W. Y., Deng Palomares, M. L., Watson, R. and Pauly, D. (2012). Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nature Climate Change 3, 254-258.

Pörtner, H. O. and Knust, R. (2006). Climate Change Affects Marine Fishes Through the Oxygen Limitation of Thermal Tolerance. Science315, 95-97.

Weibel, E. R., Taylor, C. R. and Hoppeler, H. (1991). The concept of symmorphosis: a testable hypothesis of structure-function relationship. Science, 88,10357-10361.

Tags: ocltt, respiration, thermal tolerance

Posted on: 25th July 2019 , updated on: 15th August 2019

Read preprint (1 votes)




  • Author's response

    Brad A. Seibel shared

    Charlotte,  Thanks for choosing our paper to highlight and for your excellent summary.

    • How do species that are known as ‘living fossils’ fit into this framework? Does this relationship still hold for archaic species which have changed little in recent history?

    We believe this framework applies to at least all species with circulatory systems, regardless of their evolutionary history. That said, there are many open questions remaining. For example, Pcrit for the MMR (Pcrit-max) is rarely measured. Our analysis suggests that for most shallow aquatic and terrestrial animals, that Pcrit-max is near air-saturation (21 kPa). However, this should be measured directly across a range of oxygen values including hyperoxia.  Also, the mechanistic basis of the proposed relationships is unclear.  Lastly, we have very little data for animals without obvious oxygen supply systems and those heavily dependent upon simple diffusion (e.g. jellyfish, skin-breathing amphibians and microbes).

    • How do characteristics such as the Root effect observed in teleost hemoglobins play into this relationship?

    The key is that the relationship between environmental PO2and blood-oxygen saturation must be approximately linear. Linearity is a bit surprising given the complexities in the relationships between arterial POand pH, haemoglobin oxygen affinity and total capacity, temperature, environmental oxygen and exercise. Our theory suggests that all of these things interact to preserve a linear relationship, providing a constant amount of oxygen per unit environmental PO2.

    • How can this new relationship help to inform how species may react to global climate change, and can we use it to mitigate effects or manage populations more successfully?

    The ability to predict changing species’ distributions with climate was a major driver of this work and the preceding paper describing a Metabolic Index (Deutsch et al., 2015). That work showed that the Metabolic Index (effectively a measure of potential factorial aerobic scope) declines with temperature to a fairly conserved value near 2 to 3 across species. We initially interpreted this as a limiting factor for population maintenance.  When temperature increases or oxygen declines beyond the levels providing a factorial aerobic scope of ~3, species abundances decline.  Now, with the present work, we understand that aerobic scope is not limiting. Rather species have evolutionarily adjusted oxygen supply capacity to provide an aerobic scope of at least 2 to 3 within their native habitat.  Beyond that upper temperature, there has been no selection to maintain any physiological system.  In other words, existing upper temperatures, like oxygen values, are the evolved limit. Any decline in oxygen or any increase in temperature beyond the ranges to which species have evolved reduces factorial aerobic scope, increases the likelihood of systemic failure and reduces maximum performance.  All species have apparently evolved to have a similar factorial aerobic scope (~6-3) across their native temperature range.  So we can use the temperature coefficients for basal or resting metabolic rate and the critical POto predict the approximate maximum temperature that produces that minimum aerobic scope.  There are sure to be exceptions, but we believe it will be applicable across a wide range of marine and terrestrial animals.

    • If oxygen supply capacity has evolved to match oxygen availability, then why is CTmax generally higher than any temperature experienced by an animal?

    In our paper, we defined CTmax as the temperature providing a factorial aerobic scope of 1 (where MMR meets BMR or where Pcrit meets Pcrit-max, which is air-saturation for most shallow and terrestrial animals).  As discussed above, most species fail at temperatures much lower than that (at a factorial aerobic scope of 2 to 3).  That higher factorial aerobic scope reflects the requirement of animals for some level of activity and energy beyond simple maintenance (beyond BMR).  CTmax has also been defined operationally as the temperature inducing physiological failure of one system or another.  Those two definitions are not related and have led to much confusion.  Physiological failure may occur at any temperature beyond the native habitat and have nothing to do with oxygen supply or metabolic rate.

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