Hypoxia Tolerance of 10 Euphausiid Species in Relation to Vertical Temperature and Oxygen Gradients

Oxygen Minimum Zones prevail in most of the world’s oceans and are particularly extensive in Eastern Boundary Upwelling Ecosystems such as the Humboldt and the Benguela upwelling systems. In these regions, euphausiids are an important trophic link between primary producers and higher trophic levels. The species are known as pronounced diel vertical migrators, thus facing different levels of oxygen and temperature within a 24 h cycle. Declining oxygen levels may lead to vertically constrained habitats in euphausiids, which consequently will affect several trophic levels in the food web of the respective ecosystem. By using the regulation index (RI), the present study aimed at investigating the hypoxia tolerances of different euphausiid species from Atlantic, Pacific as well as from Polar regions. RI was calculated from 141 data sets and used to differentiate between respiration strategies using median and quartile (Q) values: low degree of oxyregulation (0.25 0.25 or Q3 > 0.75); and metabolic suppression (RI median, Q1 and Q3 0) was identified for the neritic temperate species Thysanoessa spinifera and the tropical species Euphausia lamelligera. RI values of Euphausia distinguenda and the Humboldt species Euphausia mucronata qualified these as metabolic suppressors. RI showed a significant impact of temperature on the respiration strategy of E. hanseni from oxyregulation to metabolic suppression. The species’ estimated hypoxia tolerances and the degree of oxyconformity vs. oxyregulation were linked to diel vertical migration behavior and the temperature experienced during migration. The results highlight that the euphausiid species investigated have evolved various strategies to deal with different levels of oxygen, ranging from species showing a high degree of oxyconformity to strong oxyregulation. Neritic species may be more affected by hypoxia, as these are often short-distance-migrators and only adapted to a narrow range of environmental conditions

Overwintering individuals of the Arctic krill Thysanoessa inermis appear tolerant to short-term exposure to low pH conditions

Areas of the Arctic Ocean are already experiencing seasonal variation in low pH/elevated pCO2 and are predicted to be the most affected by future ocean acidification (OA). Krill play a fundamental ecological role within Arctic ecosystems, serving as a vital link in the transfer of energy from phytoplankton to higher trophic levels. However, little is known of the chemical habitat occupied by Arctic invertebrate species, and of their responses to changes in seawater pH. Therefore, understanding krill’s responses to low pH conditions has important implications for the prediction of how Arctic marine communities may respond to future ocean change. Here, we present natural seawater carbonate chemistry conditions found in the late polar winter (April) in Kongsfjord, Svalbard (79°North) as well as the response of the Arctic krill, Thysanoessa inermis, exposed to a range of low pH conditions. Standard metabolic rate (measured as oxygen consumption) and energy metabolism markers (incl. adenosine triphosphate (ATP) and l-lactate) of T. inermis were examined. We show that after a 7 days experiment with T. inermis, no significant effects of low pH on MO2, ATP and l-lactate were observed. Additionally, we report carbonate chemistry from within Kongsfjord, which showed that the more stratified inner fjord had lower total alkalinity, higher dissolved inorganic carbon, pCO2 and lower pH than the well-mixed outer fjord. Consequently, our results suggest that overwintering individuals of T. inermis may possess sufficient ability to tolerate short-term low pH conditions due to their migratory behaviour, which exposes T. inermis to the naturally varying carbonate chemistry observed within Kongsfjord, potentially allowing T. inermis to tolerate future OA scenarios

Marine meso-herbivore consumption scales faster with temperature than seaweed primary production, supplementary material

Respiration of ectotherms is predicted to increase faster with rising environmental temperature than photosynthesis of primary producers because of the differential temperature dependent kinetics of the key enzymes involved. Accordingly, if biological processes at higher levels of complexity are constrained by underlying metabolic functions food consumption by heterotrophs should increase more rapidly with rising temperature than photo-autoptrophic primary production. We compared rates of photosynthesis and growth of the benthic seaweed Fucus vesiculosus with respiration and consumption of the isopod Idotea baltica to achieve a mechanistic understanding why warming strengthens marine plant-herbivore interactions. In laboratory experiments thallus pieces of the seaweed and individuals of the grazer were exposed to constant temperatures at a range from 10 to 20°C. Photosynthesis of F. vesiculosus did not vary with temperature indicating efficient thermal acclimation whereas growth of the algae clearly increased with temperature. Respiration and food consumption of I. baltica also increased with temperature. Grazer consumption scaled about 2.5 times faster with temperature than seaweed production. The resulting mismatch between algal production and herbivore consumption may result in a net loss of algal tissue at elevated temperatures. Our study provides an explanation for faster decomposition of seaweeds at elevated temperatures despite the positive effects of high temperatures on algal growth

Responses of the arcto-boreal krill species Thysanoessa inermis to variations in water temperature: coupling Hsp70 isoform expressions with metabolism

Recent studies have indicated a metabolic temperature sensitivity in both the arcto-boreal krill species Thysanoessa inermis and Thysanoessa raschii that may determine these species' abundance and population persistence at lower latitudes (up to 40° N). T. inermis currently dominates the krill community in the Barents Sea and in the high Arctic Kongsfjord. We aimed to increase the knowledge on the upper thermal limit found in the latter species by estimating the CT50 value (19.7 °C) (critical temperature at which 50 % of animals are reactive) and by linking metabolic rate measurements with molecular approaches. Optical oxygen sensors were used to measure respiration rates in steps of 2 °C (from 0 to 16 °C). To follow the temperature-mediated mechanisms of passive response, i.e., as a proxy for molecular stress, molecular chaperone heat shock protein 70 (Hsp70) sequences were extracted from a transcriptome assembly, and the gene expression kinetics were monitored during an acute temperature exposure to 6 or 10 °C with subsequent recovery at 4 °C. Our results showed upregulation of hsp70 genes, especially the structurally constitutive and mitochondrial isoforms. These findings confirmed the temperature sensitivity of T. inermis and showed that the thermal stress took place before reaching the upper temperature limit estimated by respirometry at 12 °C. This study provides a baseline for further investigations into the thermal tolerances of arcto-boreal Thysanoessa spp. and comparisons with other krill species under different climatic regimes, especially Antarctica

Hypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cycles

The effects of regional variations in oxygen and temperature levels with depth were assessed for the metabolism and hypoxia tolerance of dominant euphausiid species. The physiological strategies employed by these species facilitate prediction of changing vertical distributions with expanding oxygen minimum zones and inform estimates of the contribution of vertically migrating species to biogeochemical cycles. The migrating species from the Eastern Tropical Pacific (ETP), Euphausia eximia and Nematoscelis gracilis , tolerate a Partial Pressure (PO 2 ) of 0.8 kPa at 10 °C (∼15 µM O 2 ) for at least 12 h without mortality, while the California Current species, Nematoscelis difficilis , is incapable of surviving even 2.4 kPa PO 2 (∼32 µM O 2 ) for more than 3 h at that temperature. Euphausia diomedeae from the Red Sea migrates into an intermediate oxygen minimum zone, but one in which the temperature at depth remains near 22 °C. Euphausia diomedeae survived 1.6 kPa PO 2 (∼22 µM O 2 ) at 22 °C for the duration of six hour respiration experiments. Critical oxygen partial pressures were estimated for each species, and, for E. eximia , measured via oxygen consumption (2.1 kPa, 10 °C, n = 2) and lactate accumulation (1.1 kPa, 10 °C). A primary mechanism facilitating low oxygen tolerance is an ability to dramatically reduce energy expenditure during daytime forays into low oxygen waters. The ETP and Red Sea species reduced aerobic metabolism by more than 50% during exposure to hypoxia. Anaerobic glycolytic energy production, as indicated by whole-animal lactate accumulation, contributed only modestly to the energy deficit. Thus, the total metabolic rate was suppressed by ∼49–64%. Metabolic suppression during diel migrations to depth reduces the metabolic contribution of these species to vertical carbon and nitrogen flux (i.e., the biological pump) by an equivalent amount. Growing evidence suggests that metabolic suppression is a widespread strategy among migrating zooplankton in oxygen minimum zones and may have important implications for the economy and ecology of the oceans. The interacting effects of oxygen and temperature on the metabolism of oceanic species facilitate predictions of changing vertical distribution with climate change

Thermal constraints on the respiration and excretion rates of krill, Euphausia hanseni and Nematoscelis megalops, in the northern Benguela upwelling system off Namibia

Rates of respiration and ammonia excretion of Euphausia hanseni and Nematoscelis megalops were determined experimentally at four temperatures representative of conditions encountered by these euphausiid species in the northern Benguela upwelling environment. The respiration rate increased from 7.7 μmol O2 h–1 gww–1 at 5 °C to 18.1 μmol O2 h–1 gww –1 at 20 °C in E. hanseni and from 7.0 μmol O2 h–1 gww–1 (5 °C) to 23.4 μmol O2 h–1 gww –1 (20 °C) in N. megalops. The impact of temperature on oxygen uptake of the two species differed significantly. Nematoscelis megalops showed thermal adaptations to temperatures between 5 °C and 10 °C (Q10 = 1.9) and metabolic constraint was evident at higher temperatures (Q10 = 2.6). In contrast, E. hanseni showed adaptations to temperatures of 10–20 °C (Q10 = 1.5) and experienced metabolic depression below 10 °C (Q10 = 2.6). Proteins were predominantly metabolised by E. hanseni in contrast to lipids by N. megalops. Carbon demand of N. megalops between 5 and 15 °C was lower than in E. hanseni versus equal food requirements at 20 °C. It is concluded that the two species display different physiological adaptations, based on their respective temperature adaptations, which are mirrored in their differential vertical positioning in the water column