Description: Ocean acidification is hypothesized to limit the performance of squid owing to their exceptional oxygen demand and pH sensitivity of blood–oxygen binding, which may reduce oxygen supply in acidified waters. The critical oxygen partial pressure (Pcrit), the PO2 below which oxygen supply cannot match basal demand, is a commonly reported index of hypoxia tolerance. Any CO2-induced reduction in oxygen supply should be apparent as an increase in Pcrit. In this study, we assessed the effects of CO2 (46–143 Pa; 455–1410 μatm) on the metabolic rate and Pcrit of two squid species - Dosidicus gigas and Doryteuthis pealeii – through manipulative experiments. We also developed a model, with inputs for hemocyanin pH sensitivity, blood PCO2 and buffering capacity, that simulates blood oxygen supply under varying seawater CO2 partial pressures. We compare model outputs with measured Pcrit in squid. Using blood–O2 parameters from the literature for model inputs, we estimated that, in the absence of blood acid–base regulation, an increase in seawater PCO2 to 100 Pa (1000 μatm) would result in a maximum drop in arterial hemocyanin–O2 saturation by 1.6% at normoxia and a Pcrit increase of 0.5 kPa. Our live-animal experiments support this supposition, as CO2 had no effect on measured metabolic rate or Pcrit in either squid species.

Description: The jumbo squid, Dosidicus gigas, can survive extended forays into the oxygen minimum zone (OMZ) of the Eastern Pacific Ocean. Previous studies have demonstrated reduced oxygen consumption and a limited anaerobic contribution to ATP production, suggesting the capacity for substantial metabolic suppression during hypoxic exposure. Here, we provide a more complete description of energy metabolism and explore the expression of proteins indicative of transcriptional and translational arrest that may contribute to metabolic suppression. We demonstrate a suppression of total ATP demand under hypoxic conditions (1% oxygen, PO2=0.8 kPa) in both juveniles (52%) and adults (35%) of the jumbo squid. Oxygen consumption rates are reduced to 20% under hypoxia relative to air-saturated controls. Concentrations of arginine phosphate (Arg-P) and ATP declined initially, reaching a new steady state (~30% of controls) after the first hour of hypoxic exposure. Octopine began accumulating after the first hour of hypoxic exposure, once Arg-P breakdown resulted in sufficient free arginine for substrate. Octopine reached levels near 30 mmol g−1 after 3.4 h of hypoxic exposure. Succinate did increase through hypoxia but contributed minimally to total ATP production. Glycogenolysis in mantle muscle presumably serves to maintain muscle functionality and balance energetics during hypoxia. We provide evidence that post-translational modifications on histone proteins and translation factors serve as a primary means of energy conservation and that select components of the stress response are altered in hypoxic squids. Reduced ATP consumption under hypoxia serves to maintain ATP levels, prolong fuel store use and minimize the accumulation of acidic intermediates of anaerobic ATP-generating pathways during prolonged diel forays into the OMZ. Metabolic suppression likely limits active, daytime foraging at depth in the core of the OMZ, but confers an energetic advantage over competitors that must remain in warm, oxygenated surface waters. Moreover, the capacity for metabolic suppression provides habitat flexibility as OMZs expand as a result of climate change.