A new analysis of hypoxia tolerance in fishes using a database of critical oxygen level (P crit)

Abstract

Hypoxia is a common occurrence in aquatic habitats, and it is becoming an increasingly frequent and widespread environmental perturbation, primarily as the result of anthropogenic nutrient enrichment and climate change. An in-depth understanding of the hypoxia tolerance of fishes, and how this varies among individuals and species, is required to make accurate predictions of future ecological impacts and to provide better information for conservation and fisheries management. The critical oxygen level (P crit) has been widely used as a quantifiable trait of hypoxia tolerance. It is defined as the oxygen level below which the animal can no longer maintain a stable rate of oxygen uptake (oxyregulate) and uptake becomes dependent on ambient oxygen availability (the animal transitions to oxyconforming). A comprehensive database of P crit values, comprising 331 measurements from 96 published studies, covering 151 fish species from 58 families, provides the most extensive and up-to-date analysis of hypoxia tolerance in teleosts. Methodologies for determining P crit are critically examined to evaluate its usefulness as an indicator of hypoxia tolerance in fishes. Various abiotic and biotic factors that interact with hypoxia are analysed for their effect on P crit, including temperature, CO2, acidification, toxic metals and feeding. Salinity, temperature, body mass and routine metabolic rate were strongly correlated with P crit; 20% of variation in the P crit data set was explained by these four variables. An important methodological issue not previously considered is the inconsistent increase in partial pressure of CO2 within a closed respirometer during the measurement of P crit. Modelling suggests that the final partial pressure of CO2 reached can vary from 650 to 3500 µatm depending on the ambient pH and salinity, with potentially major effects on blood acid-base balance and P crit itself. This database will form part of a widely accessible repository of physiological trait data that will serve as a resource to facilitate future studies of fish ecology, conservation and management.

Keywords: Carbon dioxide; critical oxygen tension; metabolic rate; oxygen and capacity limitation of thermal tolerance; physiological trait.

Figure 1:

Diagram illustrating the conceptual idea of the effects of hypoxia on the standard metabolic rate (SMR), routine metabolic rate (RMR), maximal metabolic rate (MMR) and aerobic scope (AS) of an oxyregulator. This and may not apply to species with facultative metabolic depression below the critical oxygen level (P_crit). Pc_max is defined as the critical exeternal oxygen partial pressure at which oxygen supply no longer meets the maximum demand for oxygen (Portner, 2010).

Figure 2:

Model of the estimated partial pressure of carbon dioxide ($P_{\mathrm{C}{\mathrm{O}}_2}$) reached, in water of different salinities and starting pH values, after the addition of 140 µM CO₂. The value of 140 µM approximates the increase in total CO₂ attributable to excretion by a fish at 15°C during a closed respirometry experiment. In this theoretical example, the oxygen level is allowed to decline as a result of respiration from a normoxic partial pressure of >20 kPa (∼245 µM) to a common P_crit value of ∼6 kPa (∼74 µM), and we have assumed a respiratory quotient (CO₂ excreted ÷ O₂ consumed) of 0.85 for fish (Kieffer et al., 1998). At each starting pH, the total alkalinity (TA) and total CO₂ were calculated from the pH and assuming equilibration with atmospheric $P_{\mathrm{C}{\mathrm{O}}_2}$ (395 µatm). When excreted CO₂ is dissolved in water, the total CO₂ increases accordingly (in this case, by 140 µM) but TA remains unchanged (Riebesell et al., 2010). For each starting pH, we therefore used the CO2sys program (for the national bureau of standards pH scale) to calculate the final $P_{\mathrm{C}{\mathrm{O}}_2}$ that would result from increasing total CO₂ by 140 µM while TA remained constant. This was repeated for salinities of 20, 25, 30, 35 and 40 practical salinity units (PSU) and starting pH values of 7.5–8.5 to cover ranges experienced in many marine laboratories.

Figure 3:

The effect of temperature on inter-species critical oxygen level (P_crit; black dashed line) and intra-species P_crit (continuous lines).

Figure 4:

The effect of environmental salinity on inter-species critical oxygen level (P_crit), expressed as partial pressure of oxygen (in kilopascals; A) and concentration of oxygen (in milligrams per litre; B). Data are shown as means + SEM, including data from 82 species in seawater and 50 species in freshwater. *Unpaired t-test, significant when P < 0.050.