Tolerance mechanisms and responses of krill species of different latitudes to oxygen minimum zones

Abstract

Euphausiids (krill) constitute a major part of the macrozooplankton community in terms of total biomass and play a key role in the food webs of the most productive marine ecosystems of the world. The physiological strategies and OMZ tolerance mechanisms of euphausiids on a global-scale were investigated to explain the current zoogeographical pattern of major species and project it in the future. A global euphausiid respiration ANN (Artificial Neural Network) model was built with 2479 data sets enclosing 23 of the total 86 species. The model included the effect of latitude (LAT), the day of the year (DoY), and the number of daylight hours (DLh), in addition to the basal variables that determine ectothermal oxygen consumption (temperature, body mass and depth). The ANN model indicated a decrease in respiration with increasing LAT and decreasing DLh. Respiratory measurements and experiments combining hypoxia/reoxygenation exposure coupled with warming were conducted to understand adaptation of species to OMZs. Euphausia mucronata from the Humboldt Current system (HCS) starts metabolic suppression below 80% oxygen (O2) saturation (18 kPa) showing adaptation to OMZ conditions. Euphausia pacifica and the Antarctic krill, Euphausia superba, were characterized as oxyregulators and maintain respiration rates constant down to 30% (6 kPa) and 55% O2 (10 kPa) saturation, respectively. E. mucronata and E. pacifica had higher SOD (superoxide dismutase) values in winter than in summer, which relate to higher winter metabolic rate (in E. pacifica). Normoxic subsurface oxygenation in the HCS during winter already poses a high oxygen stress for E. mucronata. In winter, when temperature is homogenous and the OMZ absent, a 4°C warming combined with hypoxia represents a lethal condition for E. pacifica. Climate change scenario combining warming and hypoxia thus represents a serious threat to E. pacifica and, as a consequence, to its habitat food webs. Antarctic krill had the lowest antioxidant enzyme activities, but the highest concentrations of the molecular antioxidant glutathione (GSH) and was not lethally affected by 6 h exposure to moderate hypoxia. Gene expression related to aerobic metabolism, antioxidant defence, and heat- shock response under severe (2.5% O2 saturation or 0.6 kPa) and threshold (20% O2 saturation or 4 kPa) hypoxia exposure was investigated to detect aspects of the molecular stress response. Expression levels of the genes citrate synthase (CS), mitochondrial manganese superoxide dismutase (SODMn-m) and the heat-shock protein isoform (E) were higher in euphausiids incubated 6 h at 20% O2 saturation than in animals exposed to normoxic conditions. The transcription is likely to prepare the krill for eventual reoxygenation, which connects with the swarming behaviour of this species. This cold-adapted species thus possesses the cellular tools from its sub-polar ancestor to tolerate levels of hypoxia severer than the oxygen concentration of its habitat.