Ocean deoxygenation and zooplankton: Very small oxygen differences matter.

Oxygen minimum zones (OMZs), large midwater regions of very low oxygen, are expected to expand as a result of climate change. While oxygen is known to be important in structuring midwater ecosystems, a precise and mechanistic understanding of the effects of oxygen on zooplankton is lacking. Zooplankton are important components of midwater food webs and biogeochemical cycles. Here, we show that, in the eastern tropical North Pacific OMZ, previously undescribed submesoscale oxygen variability has a direct effect on the distribution of many major zooplankton groups. Despite extraordinary hypoxia tolerance, many zooplankton live near their physiological limits and respond to slight (≤1%) changes in oxygen. Ocean oxygen loss (deoxygenation) may, thus, elicit major unanticipated changes to midwater ecosystem structure and function.

Light-limitation on predator-prey interactions: consequences for metabolism and locomotion of deep-sea cephalopods.

The present study attempts to correlate the metabolism and locomotory behavior of 25 species of midwater Cephalopoda from California and Hawaii with the maximal activities of key metabolic enzymes in various locomotory muscle tissues. Citrate synthase (CS) and octopine dehydrogenase (ODH) activities were used as indicators of aerobic and anaerobic metabolic potential respectively. CS activity in mantle muscle is highly correlated with whole-animal rates of oxygen consumption, whereas ODH activity in mantle muscle is significantly correlated with a species' ability to buffer the acidic end-products of anaerobic metabolism. Both CS and ODH activities in mantle muscle declined strongly with a species' habitat depth. For example, CS and ODH activities ranged respectively from 0.04 units g(-1) and 0.03 units g(-1) in the deep-living squid Joubiniteuthis portieri, to 8.13 units g(-1) and 420 units g(-1) in the epipelagic squid Sthenoteuthis oualaniensis. The relationships between enzymatic activities and depth are consistent with similar patterns observed for whole-animal oxygen consumption. This pattern is believed to result from a relaxation, among deep-living species, in the need for strong locomotory abilities for visual predator/prey interactions; the relaxation is due to light-limitation in the deep sea. Intraspecific scaling patterns for ODH activities may, for species that migrate ontogenetically to great depths, reflect the counteracting effects of body size and light on predator-prey detection distances. When scaled allometrically, enzymatic activities for the giant squid, Architeuthis sp., suggest a fairly active aerobic metabolism but little burst swimming capacity. Interspecific differences in the relative distributions of enzymatic activities in fin, mantle, and arm tissue suggest an increased reliance on fin and arm muscle for locomotion among deep-living species. We suggest that, where high-speed locomotion is not required, more efficient means of locomotion, such as fin swimming or medusoid arm propulsion, are more prevalent.

Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers.

Zones of minimum oxygen level are found at intermediate depths in most of the world's oceans and, although the oxygen partial pressure in some of these 'oxygen minimum layers' is only a fraction of a kilopascal, populations of pelagic metazoans exist there. These oxygen minimum layers are areas of the water column and the associated benthos with stable conditions of continuously low oxygen level and low temperature at intermediate depths (400-1000 m depth) over vast areas. Off California, where PO2 at the oxygen minimum is 0.8 kPa, there are abundant populations of animals both in the water column and on the bottom. Farther to the south in the eastern tropical Pacific, oxygen partial pressures of less than approximately 0.4 kPa result in very low biomasses and diversity of animals at minimum layer depths. At the minimum oxygen levels found off California, most animals which inhabit the minimum zones appear to support their routine metabolic demands via aerobic metabolism. They do this by being very effective at removing oxygen from water. Among the adaptations of pelagic crustaceans to these conditions are: (1) enhanced ventilatory abilities, (2) enhanced percentage removal of O2 from the ventilatory stream, (3) large gill surface areas, (4) short diffusion distances from the water to the blood, and (5) hemocyanin respiratory proteins with a very high affinity for O2, high cooperativity and large Bohr effects. The lower O2 consumption rates of many deeper-living species are also functionally adaptive in that they facilitate aerobic survival at low PO2. However, they are not adaptations to the minimum layer, since similarly low rates are found in the same and comparable species living at the same depths in regions without well-developed minima, and these animals are unable to survive at the low PO2 values of the minima. While anaerobic metabolism may be important for metabolic rates above the routine level for most animals in the minimum layer, there is little evidence for the use of sustained anaerobiosis in the species studied. In summary, given the stable presence of very low O2 levels in the minima, the primary adaptations of animals living within them are those that support aerobic metabolism by giving the animals remarkable abilities to extract O2 from water. These abilities are notably better than those of animals adapted to unstable hypoxic environments, such as intertidal mudflats, while the latter animals rely to a much greater extent on anaerobiosis and perhaps on metabolic suppression to survive periods of anoxia.

Decline in Pelagic Cephalopod Metabolism With Habitat Depth Reflects Differences in Locomotory Efficiency.

The metabolic rates of 33 species of pelagic cephalopods from California and Hawaii were measured and correlated with minimum depth of occurrence. Mean metabolic rates ranged from 0.07 {mu}mol O2g-1 h-1 for the deep-living vampire squid, Vampyroteuthis infernalis, to 8.79 {mu}mol O2 g-1 h-1 for Gonatus onyx, a vertically migrating squid. An individual of V. infernalis, which lives within the oxygen minimum layer off California, had the lowest mass-specific metabolic rate ever measured for a cephalopod (0.02 {mu}mol O2g-1 h-1, 1050 g wet weight). For species collected in sufficient quantity and size range, metabolism was related to body size. Critical partial pressures of oxygen (Pc) were determined for Hawaiian and Californian cephalopods. Pc values for Hawaiian animals were considerably higher than for those taken off California, a trend that corresponds to the higher levels of environmental oxygen in the Hawaiian waters. Buffering capacity ({beta}) of mantle muscle, assayed in eight cephalopod species, was used to estimate the capacity for glycolytic energy production. Mean {beta} ranged from 1.43 slykes for a bathypelagic octopod, Japetella heathi, to 77.08 slykes for an epipelagic squid. Sthenoteuthis oualaniensis. Significant declines with increasing depth of occurrence were observed for both metabolism and {beta}. The decline in metabolic parameters with depth is interpreted as a decreased reliance on locomotory abilities for predator/prey interactions in the light-limited deep sea. The decline in metabolism with depth observed for pelagic cephalopods was significantly steeper than that previously observed for either pelagic fishes or crustaceans. We suggest that since strong locomotory abilities are not a priority in the deep sea, deeper-living cephalopods may rely more heavily on means of locomotion that are more efficient than jet propulsion via mantle contractions--means such as fin swimming or medusoid swimming utilizing the arms and extensive webbing present in many deep-living species. The greater efficiency of deeper-living cephalopods may be responsible for the observation that the decline in metabolic rates with depth is more pronounced for pelagic cephalopods than for fishes or crustaceans.