The real limits to marine life: a further critique of the Respiration Index

Abstract

The recently proposed "Respiration Index" (RI = log <i>P</i>O₂/<i>P</i>CO₂) suggests that aerobic metabolism is limited by the ratio of reactants (oxygen) to products (carbon dioxide) according to the thermodynamics of cellular respiration. Here, we demonstrate further that, because of the large standard free energy change for organic carbon oxidation (&Delta;<i>G</i>&deg; = −686 kcal mol⁻¹), carbon dioxide can never reach concentrations that would limit the thermodynamics of this reaction. A <i>P</i>CO₂ to <i>P</i>O₂ ratio of 10⁵⁰³ would be required to reach equilibrium (equilibrium constant, <i>K</i>_eq = 10⁵⁰³), where &Delta;<i>G</i> = 0. Thus, a Respiration Index of −503 would be the real thermodynamic limit to aerobic life. Such a Respiration Index is never reached, either in the cell or in the environment. Moreover, cellular respiration and oxygen provision are kinetically controlled such that, within limits, environmental oxygen and CO₂ concentrations have little to do with intracellular concentrations. The RI is fundamentally different from the aragonite saturation state, a thermodynamic index used to quantify the potential effect of CO₂ on calcification rates, because of its failure to incorporate the equilibrium constant of the reaction. Not only is the RI invalid, but its use leads to incorrect and misleading predictions of the threat of changing oxygen and carbon dioxide to marine life. We provide a physiological framework that identifies oxygen thresholds and allows for synergistic effects of ocean acidification and global warming

Synergistic effects of hypoxia and increasing CO2 on benthic invertebrates of the central Chilean coast

“…Our results show that metabolic rates decline with decreasing RI, as expected (Brewer and Peltzer, 2009), confirming that the RI holds power as a predictor of effects, separate or combined, of hypoxia and high CO 2 on metabolic rates. However, our results also support the criticisms of Seibel and Childress (2013) to the predictive power of the thresholds proposed by Brewer and Peltzer (2009). The lowest RI we reached in our experiment was 0.81 ± 0.06, reached in the L O2 H CO2 treatment.…”

“…The additive nature of the effects of hypoxia and high CO 2 lends weight to the use of the Respiration Index, RI, to reflect their combined stress on metabolic processes. Whereas the merit of the RI has been challenged recently (Seibel and Childress, 2013) no experimental test had been reported to date. Our results show that metabolic rates decline with decreasing RI, as expected (Brewer and Peltzer, 2009), confirming that the RI holds power as a predictor of effects, separate or combined, of hypoxia and high CO 2 on metabolic rates.…”

“…However, the RI index has not been experimentally tested and the underlying expectations have been criticized. Seibel and Childress (2013) argue that CO 2 could never reach concentrations that would limit the thermodynamics of this reaction, because of the large standard free energy change for organic carbon oxidation ( G • = −686 kcal mol −1 ), and that a PCO 2 :PO 2 ratio of 10503 would be required to reach equilibrium (equilibrium constant, K eq = 10503; where G = 0). Thus, they argued that a RI of −503 would be the real thermodynamic limit to aerobic life.…”

“…Thus, they argued that a RI of −503 would be the real thermodynamic limit to aerobic life. Although it has been shown that in crabs and catfish the pCO 2 in plasma dropped to 45 and 56 mm Hg, respectively, when exposed to elevated CO 2 , Pörtner et al (2005), Seibel and Childress (2013), and Cameron and Iwama (1989) argue that cellular respiration and oxygen provision are kinetically controlled and environmental oxygen and CO 2 concentrations exert little control on intracellular concentrations. Yet, evidence for synergistic effects of low O 2 and high CO 2 includes increased bacterial infections in the pacific white shrimp Litopenaeus vannamei (Burgents et al, 2005), inhibition of growth and metamorphosis in the early life stage of bivalves (bay scallops, Argopecten irradians, and hard clams, Mercenaria mercenaria, Gobler et al, 2014), depressed growth rates for juvenile red abalone (Haliotis rufescens, Kim et al, 2013) and synergistic metabolic depression via the effect of adenosine on central nervous functions of the marine invertebrate Sipunculus nudus (Reipschläger et al, 1997;Pörtner et al, 2005).…”

Ecophysiological limits to aerobic metabolism in hypoxia determine epibenthic distributions and energy sequestration in the northeast Pacific ocean

“…Although the metabolic relationship between oxygen demand and [O 2 ] env availability is well-established, few studies have applied O crit 2 as a tool for assessing ecological response of in situ distributions (Deutsch et al 2015). O crit 2 values remain unknown for most marine species (Seibel and Childress 2013) and are uncoupled from field abundance data which rarely have in situ, concomitant measurements of [O 2 ] env . Furthermore, no integrative datasets exist for the Pacific Ocean-areas of which are the most susceptible to aerobic habitat loss in the future (Deutsch et al 2015).…”