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Species that are able to maintain an aerobic existence in oxygen minima do so by having a highly effective system for removing oxygen from seawater, allowing them to consume oxygen in sufficient quantities to sustain life at very low oxygen concentrations. The ability to regulate oxygen consumption down to very low levels of external oxygen is defined in physiological terms as having a low critical oxygen partial pressure, or P_c. Figure 2.22 shows the relationship of oxygen consumption rate and external PO₂ for an oxygen‐minimum‐layer species, the shrimp‐like lophogastrid Gnathophausia (now Neognathophausia) ingens. The species is able to regulate its oxygen consumption (VO₂) down to the lowest oxygen level it experiences in its environment in the oxygen minimum layer off the coast of California (8 mm Hg oxygen or 0.8 kPa). The P_c is the point on the curves where the oxygen consumption declines precipitously toward 0 and it varies with activity level as shown. A study on the relationship of species’ critical oxygen partial pressures vs. their minimum environmental PO₂ shows that for most oxygen minimum dwellers, species’ P_cs are equivalent to the lowest oxygen concentrations encountered in nature (Childress and Seibel 1998). What is surprising is that all pelagic species living in normoxic waters that have been examined can also regulate their oxygen consumption down to a low PO₂: 4–6 kPa, or 20–30% of air saturation (Childress 1975; Donnelly and Torres 1988; Cowles et al. 1991; Torres et al. 1994). Thus, even at very much higher habitat O₂ levels, pelagic species maintain a P_c near 4 kPa. It is tempting to conclude that 4 kPa reflects a global ocean oxygen minimum that had to be accommodated by most pelagic species at some point during geological history. While possible, evidence does not support it (Childress and Seibel 1998). What is more likely is that the occasional high oxygen demands of increased activity and the respiratory machinery it requires coincidentally equip most species with the ability to take up and transport oxygen down to 4 kPa.

Figure 2.22 Oxygen consumption rate of the lophogastrid Gnathophausia ingens as a function of oxygen concentration (in milliliters of oxygen per liter). Open circles represent a single very active animal; closed circles represent the mean of 23 runs with 8 individuals; closed triangles represent a single non‐swimming animal. The vertical lines represent plus or minus one standard deviation.

Source: J. J. Childress, Oxygen minimum layer: vertical distribution and respiration of the mysid Gnathophausia ingens, Science, 1968, Vol 160, Issue 3833, figure 1 (p. 1242). Reprinted with permission from AAAS.

Gnathophausia ingens has been the subject of several detailed studies by Childress and his students. Their studies paint a very complete picture of how the species copes with low oxygen. Rather than any exotic adaptations, such as unusual new respiratory structures, Gnathophausia has achieved its ability to thrive in the OMZ by very highly developed gas‐exchange and circulatory systems. Six major adaptations have been noted. First, G. ingens has a very high ventilation volume; that is, it can move a considerable amount of water over its gills per unit time: up to 81 kg min⁻¹ (Figures 2.23 and 2.24). Second, it is very efficient at removing oxygen from the ventilatory stream, even when that stream is moving very rapidly over the gills. This property is known as the % utilization of oxygen and in Gnathophausia it can be as high as 90% (Figures 2.23 and 2.24). That high % utilization is achieved through its third, fourth, and fifth adaptations: a very high gill surface area to maximize the possibility for exchange (9–14 cm² g⁻¹ wet mass); a minimal diffusion distance in the gill filaments themselves (1.5–2.5 μm) to minimize the barrier for oxygen diffusion into the blood (very unusual for Crustacea); and a very effective blood pigment (hemocyanin) capable of taking up oxygen at very low concentrations (50% saturated at 0.19 kPa). A well‐developed circulatory system rounds out the suite of adaptations with the capability of delivering 225 ml kg⁻¹ min⁻¹.

Figure 2.23 Oxygen consumption rate, percent utilization of oxygen, and ventilation volume in Gnathophausia ingens as a function of oxygen partial pressure, mean of eight runs. Solid line represents oxygen consumption rate; dotted line represents % utilization; dashed line depicts measured ventilation volume; dot‐dash line is calculated ventilation volume.

Source: Figure 4 from Childress (1971), Biol. Bull. 141: 114. Reprinted with permission from the Marine Biological Laboratory, Woods Hole, MA.

Figure 2.24 Relationship between percent utilization and ventilation volume in Gnathophausia ingens utilizing the values given in Figure 2.23.

Source: Figure 5 from Childress (1971), Biol. Bull. 141: 115. Reprinted with permission from the Marine Biological Laboratory, Woods Hole, MA.

No other oxygen‐minimum‐layer species has been examined as well as G. ingens. Taken together, the several studies on the species’ respiratory physiology paint a complete picture of how it is possible to survive at vanishingly low oxygen concentrations. Nonetheless, a few pieces of the puzzle have been collected in other taxa to suggest that elements of the suite have been employed by other species to achieve the same end. The most important characteristic to look for is a P_c at or below the lowest PO₂ encountered in nature. That characteristic has been observed in many of the Crustacea living in the oxygen minimum in the California borderland (8 mm Hg, Childress 1975; Childress and Seibel 1998). It has also been seen in at least one crustacean dwelling in the Eastern Tropical Pacific where the oxygen minimum layer is as low as 3 mm Hg O₂: the galatheid red crab Pleuroncodes planipes with a P_c of 3 mm Hg (Quetin and Childress 1976).

Once an individual reaches its P_c, it responds behaviorally and metabolically. Since metabolism scales positively with activity level, activity is minimized, precipitously dropping metabolic demand for ATP. Any ATP deficit resulting from the inability to meet its needs aerobically must be made up by anaerobic glycolysis. The hypoxia‐induced drop in activity resulting in lowered ATP demand is termed metabolic suppression (Seibel 2011; Seibel et al. 2016) and is not confined to pelagic fauna. It is the first weapon any species can wield to reduce the demand for ATP and is exploited by intertidal species, such as bivalves, during low tide exposure (Hochachka and Somero 1984; Hochachka and Guppy 1987).

Pelagic cephalopods dwelling in the California oxygen minimum also exhibit low P_cs (3–7 mm Hg, Seibel et al. 1999). Data were collected from the vampire squid Vampyroteuthis infernalis, a fulltime resident of the California borderland’s oxygen minimum zone, on two characteristics of the “Gnathophausia suite”: gill diffusion capacity and blood pigment efficiency (Table 2.4). The diffusion capacity, DGO₂, and oxygen affinity, P₅₀, of Vampyroteuthis shown in Table 2.4 are indicative of a highly efficient gas‐exchange surface and a blood pigment capable of binding oxygen at extremely low concentrations. Both are quite close to those of Gnathophausia, suggesting that, with respect to these two important physiological characteristics, the species are employing a common strategy. Data from the other cephalopod species in Table 2.4 show substantially lower gill diffusion capacity and oxygen affinity in the species inhabiting more normoxic environments.

Vampyroteuthis has a much lower metabolic rate than Gnathophausia. On a mass‐specific basis, the vampire squid’s respiratory rate is a little less than 10% that of G. ingens. On one hand, Vampyroteuthis’ lower rate makes the job of the respiratory system a little easier because the absolute amount of oxygen required per unit time is less. On the other, because of the physics of diffusion it makes little difference, the oxygen gradient between environment and organism is still a tiny one. What might be expected, a priori, in Vampyroteuthis would be a lower capability for removing oxygen in quantity. Adaptations such as very high gill surface area and a highly developed circulatory system, important for delivering oxygen in quantity to satisfy tissue demands, would likely be less in evidence. For at least one of those characteristics, gill surface area, this appears to be the case; Vampyroteuthis has only a moderate gill surface area relative to other cephalopods (Madan and Wells 1996; Seibel et al. 1999).

Table 2.4 Metabolism (VO₂ = ml O₂ kg⁻¹ min⁻¹), gill diffusion capacity (DGO₂ = ml O₂ kg⁻¹ kPa⁻¹ min⁻¹), blood‐water oxygen gradient (∆P_g = VO₂/(DGO₂; in kPa) and hemocyanin‐oxygen affinity (P₅₀ = PO₂ in kPa at 50% hemocyanin‐oxygen saturation) of Vampyroteuthis ingernalis in comparison to other cephalopods. Data for the lophogastrid crustacean, Gnathophausia ingens, are also shown.

Source: Reprinted by permission from Springer Nature Customer Service Centre GmbH: Springer Nature, Experimental Biology Online, Vampire Blood: respiratory physiology of the vampire squid (Cephalopoda: Vampyromorpha) in relation to the oxygen minimum layer, Seibel et al. (1999).

Species	VO2 a	DGO2	∆Pg	P50 b	References
Vampyroteuthis infernalis	0.04	2.32	0.02	0.47	Madan and Wells (1996), Seibel et al. (1997)
Nautilus pompilius	0.28	0.38	0.74	2.3	Brix et al. (1989), Wells et al. (1992), Eno (1994)
Octopus vulgaris	0.35	0.45	0.77	2.45	Wells and Wells (1983), Bridges (1994), Eno (1994)
Architeuthis monachis	n.a.	n.a.	n.a.	1.65	Brix et al. (1989)
Gnathophausia ingens	0.56	3.73	0.15	0.19	Belman and Childress (1976), Sanders and Childress (1990)

n.a. = not available.

^a Normalized to 5 °C assuming Q₁₀ = 2.

^b Measured at pH 7.4 near environmental temperature.

The available evidence strongly suggests that most full‐ and part‐time residents of oxygen minima rely primarily on an aerobic strategy to make a living. The suite of adaptations exhibited by Gnathophausia ingens are likely found in whole or in part in all oxygen minimum layer residents.