Description: The oxygen consumption rates and activities of key metabolic enzymes were measured and analyzed as a function of habitat depth for several species of benthic octopod (Cephalopoda: Octopoda) including a recently described hydrothermal vent endemic species. Oxygen consumption rates and citrate synthase activity, an indicator of aerobic metabolic potential, did not vary significantly with increasing habitat depth. Anaerobic metabolic potential, as evidenced by octopine dehydrogenase activity, declined significantly with increasing habitat depth. It is suggested that burst swimming abilities, and hence glycolytic potential, are not strongly selected for in the deep-sea, where visual predator-prey interactions are reduced because of light-limitation. Oxygen consumption rates for Octopus californicus and O. bimaculoides were analyzed as a function of oxygen partial pressure as well. O. californicus, which lives in the hypoxic Santa Barbara basin at 500 m depth, was able to regulate its oxygen consumption to the limit of detectable oxygen partial pressures. O. bimaculoides, an intertidal species, had a minimum critical oxygen partial pressure of 16 mmHg. It is also shown that oxygen consumption rates and oxygen consumption regulation are strongly affected by individual experiment duration (either handling stress or food deprivation). O. californicus appears to be much more strongly affected by experiment duration than is O. bimaculoides.

Description: The majority of squid families (Teuthoidea: Cephalopoda) exchange sodium for ammonium, creating a low-density fluid that imparts lift for neutral buoyancy. However, previous methods for measuring ammonium did not distinguish between NH4+ and various other amine compounds. The present study, using single column ion chromatography, reassessed the cation concentrations in several midwater cephalopod species. High NH4+ levels were confirmed for histioteuthid, cranchiid, and chiroteuthid and related squids. A strong relationship is reported between ammonium content and body mass in Histioteuthis heteropsis, suggesting a gradual accumulation of ammonium coincident with an ontogenetic migration to greater depths. The bathypelagic squids Bathyteuthis abyssicola and Bathyteuthis berryi, on the other hand, contained very little ammonium but rather contained large quantities of an as yet unidentified cation. The ecological significance of this compound is not yet known. Morphology in Bathyteuthid squids suggests that the unknown cation is contained intracellularly and so, unlike sequestered ammonia, does not diminish the space available for muscle tissue. Accordingly, protein measurements in B. berryi mantle muscle are on par with shallower-living muscular squids, and in situ submersible observations reveal strong locomotory abilities relative to other deep-water squids.

Description: The Humboldt (or jumbo) squid, Dosidicus gigas, is an active predator endemic to the Eastern Pacific that undergoes diel vertical migrations into a pronounced oxygen minimum layer (OML). Here, we investigate the physiological mechanisms that facilitate these migrations and assess the associated costs and benefits. Exposure to hypoxic conditions equivalent to those found in the OML (∼10 μM O2 at 10 °C) led to a significant reduction in the squid’s routine metabolic rate (RMR), from 8.9 to 1.6 μmol O2 g−1 h−1 (p 〈 0.05), and a concomitant increase in mantle muscle octopine levels (from 0.50 to 5.24 μmol g−1 tissue, p 〈 0.05). Enhanced glycolitic ATP production accounted for only 7.0% and 2.8% at 10 °C and 20 °C, respectively, of the energy deficit that resulted from the decline in aerobic respiration. The observed metabolic suppression presumably extends survival time in the OML by conserving the finite stores of fermentable substrate and avoiding the accumulation of the deleterious anaerobic end products in the tissues. RMR increased significantly with temperature (p 〈 0.05), from 8.9 (at 10 °C) to 49.85 μmol O2 g−1 h−1 (at 25 °C) which yielded a Q10 of 2.0 between 10 and 20 °C and 7.9 between 20 and 25 °C (p 〈 0.05). These results suggest that 25 °C, although within the normal surface temperature range in the Gulf of California, is outside this species’ normal temperature range. By following the scattering layer into oxygen-enriched shallow water at night, D. gigas may repay any oxygen debt accumulated during the daytime. The dive to deeper water may minimize exposure to stressful surface temperatures when most prey have migrated to depth during the daytime. The physiological and ecological strategies demonstrated here may have facilitated the recent range expansion of this species into northern waters where expanding hypoxic zones prohibit competing top predators.

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.