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

Nelly.Tremblay [ at ]


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. From the species found along the Eastern Pacific coastline many do not tolerate hypoxia and they do not distribute where shallow oxygen minimum zones (OMZs) prevail. Only very few species are endemic of OMZs. In my thesis, I investigated the physiological strategies and OMZ tolerance mechanisms of euphausiids on a global-scale to explain the current zoogeographical pattern of major species and project it in the future. In a first step, the basal respiration rate of the species investigated was measured. This simple measurement is one of the best proxy to identify the optimal environmental window and the metabolic requirement scale wherein the organism is. 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. For seasonality, a General Additive model (GAM) successfully integrated DLh and DoY effects on respiration rates of the Antarctic krill, Euphausia superba, yielding the minimum metabolic activity in mid-June and the maximum at the end of December. For the North Pacific krill, Euphausia pacifica, we found no effect of DLh or DoY and the results for the North Atlantic krill, Meganyctiphanes norvegica were not meaningful, because the seasonal data were insufficient. The activity of the citrate synthase, Krebs cycle enzyme, also seems to be a promising tool for euphausiid respiration prediction and should be further analysed in pair with respiration measurements to develop a model in the future. The results emphasize that respiration measurements of Euphausiid key species should considered all seasons to improve the comparative physiological and ecological models. Respiratory measurements and experiments combining hypoxia/reoxygenation exposure coupled with warming were conducted to understand adaptation of species to OMZs. Experimental krill species had their distribution from the Antarctic to the Humboldt Current system (HCS, Chilean coast), and the Northern California Current system (NCCS, Oregon). Euphausia mucronata from the HCS starts metabolic suppression below 80% oxygen (O2) saturation (18 kPa) showing adaptation to OMZ conditions. The two species investigated in the NCCS showed different energetic strategies. Thysanoessa spinifera had a lower standard metabolic rate than Euphausia pacifica, and a respiration pattern more close to oxyconformity. Lactate accumulation, measured when the lowest oxygen partial pressure (pO2) was reached during respiratory experiment, was higher in T. spinifera, showing higher utilization of the anaerobic pathway. The NCCS krill, E. pacifica, and the Antarctic krill, E. 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). In both species, antioxidant enzyme activities remained constant during hypoxic exposure at habitat temperature. The normoxic subsurface oxygenation in the HCS during winter already poses a “high oxygen stress” for E. mucronata. Warming by 7◦C above habitat temperature in summer increased SOD activities and glutathione (GSH) levels in E. mucronata (HCS), but no oxidative damage occurred. In winter, when temperature is homogenous and the OMZ absent, a +4◦C warming combined with hypoxia represents a lethal condition for E. pacifica. In summer, when the OMZ expands upwards (100 m subsurface), antioxidant defences counteracted hypoxia and reoxygenation effects in E. pacifica, but only at mildly elevated temperature (+2◦C). Experimental warming by +4◦C reduced antioxidant activities and caused mortality of exposed specimens during the winter. Climate change scenario combining warming and hypoxia thus represents a serious threat to E. pacifica and, as a consequence, NCCS 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, indicating a good plasticity to confront future stressful conditions of other types.

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Tremblay, N. (2014): Tolerance mechanisms and responses of krill species of different latitudes to oxygen minimum zones , PhD thesis, Universität Bremen.

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