Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and³¹P-MRS

Abstract

The hypothesis of an oxygen-limited thermal tolerance was tested in the Antarctic teleost Pachycara brachycephalum. With the use of flow-through respirometry, in vivo (31)P-NMR spectroscopy, and MRI, we studied energy metabolism, intracellular pH (pH(i)), blood flow, and oxygenation between 0 and 13 degrees C under normoxia (PO(2): 20.3 to 21.3 kPa) and hyperoxia (PO(2): 45 kPa). Hyperoxia reduced the metabolic increment and the rise in arterial blood flow observed under normoxia. The normoxic increase of blood flow leveled off beyond 7 degrees C, indicating a cardiovascular capacity limitation. Ventilatory effort displayed an exponential rise in both groups. In the liver, blood oxygenation increased, whereas in white muscle it remained unaltered (normoxia) or declined (hyperoxia). In both groups, the slope of pH(i) changes followed the alpha-stat pattern below 6 degrees C, whereas it decreased above. In conclusion, aerobic scope declines around 6 degrees C under normoxia, marking the pejus temperature. By reducing circulatory costs, hyperoxia improves aerobic scope but is unable to shift the breakpoint in pH regulation or lethal limits. Hyperoxia appears beneficial at sublethal temperatures, but no longer beyond when cellular or molecular functions become disturbed.

Oxygen limited thermal tolerance in fish?

“…The shortcomings involved in studies of anaesthetized or immobilized animals were finally overcome when MRI and MRS experiments were successfully carried out in non-anaesthetized, unrestrained marine teleosts like benthic zoarcids (eelpout) or demersal gadids like Atlantic cod (Bock et al, 2001;Mark et al, 2002;Sartoris et al, 2003a,b). The experimental set-up ( Fig.…”

“…In fish, heart rate and both ventilation frequency and amplitude have frequently been reported to increase in association with a temperature-induced rise in oxygen consumption in order to compensate for elevated oxygen demand by progressively enhanced oxygen supply (Barron et al, 1987;Graham and Farrell, 1989;Mark et al, 2002). According to the concept of oxygen limited thermal tolerance (see Section 1) onset of thermal limitation should be elicited by limited capacity of oxygen supply mechanisms to match oxygen demand beyond low or high peius temperatures (T p , see above), thereby eliciting a drop in aerobic scope.…”

“…Mark et al (2002) tested whether temperature induced hypoxia was alleviated by ambient hyperoxia in the Antarctic eelpout P. brachycephalum. They monitored the effects of temperature on oxygen demand, ventilatory effort and blood flow at normoxic and hyperoxic oxygen levels (Fig.…”

Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish

“…In Antarctic stenothermal eelpout, increased HIF-1-DNA binding to the EPO-enhancer over the 0°C control levels occurred upon warming to 5°C, a temperature close to the upper tolerance limit but well tolerated by this species (Mark et al 2002a;Lannig et al 2005). Similarly, warming from 12 to 18°C (but not to above 20°C) stimulated enhanced HIF-1-DNA binding in the temperate eelpout (Heise et al 2006b).…”

“…In the stenothermal Antarctic Pachycara brachycephalum the same parameters were measured close to habitat temperature 0°C (0-0.6°C, Brodte et al 2006b), and upon several weeks of acclimation to 5°C, at the warm border of the thermal tolerance range of this Antarctic fish. Severe heat stress in this species commences at 7°C (Mark et al 2002a).…”