Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation

Lannig, Gisela; Storch, Daniela; Pörtner, Hans‐Otto

doi:10.1007/s00300-005-0730-9

Cited by 54 publications

(52 citation statements)

References 41 publications

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“…The concept of the thermal niche as a window resulting from a limited capacity for acclimatization also explains the recent observation of phenotypic plasticity in two species of Antarctic fishes, the Antarctic notothenioid Pagothenia borchgrevinki (Seebacher et al, 2005) and the Antarctic eelpout Pachycara brachycephalum (Lannig et al, 2005). In the field, the former species lives close to freezing temperatures at -1.9°C, while the latter lives at temperatures between -0.4 and +1°C (Brodte et al, 2006b).…”

Section: Acclimatizationmentioning

confidence: 88%

Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems

Pörtner

2010

Journal of Experimental Biology

1,191

984

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SummaryThe concept of oxygen-and capacity-dependent thermal tolerance in aquatic ectotherms has successfully explained climateinduced effects of rising temperatures on species abundance in the field. Oxygen supply to tissues and the resulting aerobic performance characters thus form a primary link between organismal fitness and its role and functioning at the ecosystem level. The thermal window of performance in water breathers matches their window of aerobic scope. Loss of performance reflects the earliest level of thermal stress, caused by hypoxaemia and the progressive mismatch of oxygen supply and demand at the borders of the thermal envelope. Oxygen deficiency elicits the transition to passive tolerance and associated systemic and cellular stress signals like hormonal responses or oxidative stress as well as the use of protection mechanisms like heat shock proteins at thermal extremes. Thermal acclimatization between seasons or adaptation to a climate regime involves shifting thermal windows and adjusting window widths. The need to specialize on a limited temperature range results from temperaturedependent trade-offs at several hierarchical levels, from molecular structure to whole-organism functioning, and may also support maximized energy efficiency. Various environmental factors like CO 2 (ocean acidification) and hypoxia interact with these principal relationships. Existing knowledge suggests that these factors elicit metabolic depression supporting passive tolerance to thermal extremes. However, they also exacerbate hypoxaemia, causing a narrowing of thermal performance windows and prematurely leading the organism to the limits of its thermal acclimation capacity. The conceptual analysis suggests that the relationships between energy turnover, the capacities of activity and other functions and the width of thermal windows may lead to an integrative understanding of specialization on climate and, as a thermal matrix, of sensitivity to climate change and the factors involved. Such functional relationships might also relate to climate-induced changes in species interactions and, thus, community responses at the ecosystem level.

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Section: Acclimatizationmentioning

confidence: 88%

Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems

Pörtner

2010

Journal of Experimental Biology

1,191

984

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“…Even though the thermal performance of biochemical reactions, cells, tissues, organs and organ systems may be quite disparate (Schulte, 2015), the thermal niche of a whole animal must be bounded by its critical thermal limits (T c,max and T c, min -the latter taken here as freezing point of seawater at −1.8°C, in the absence of experimental data). Yet, Antarctic stenotherms, even with a narrow window of thermal tolerance, do acclimate to warmer temperatures to some degree (Pörtner et al, 2000(Pörtner et al, , 2007Lannig et al, 2005;Seebacher et al, 2005), despite the fact that their biogeographic and thermal isolation is more extreme than that of Arctic fishes and has been this way for around 30,000 years. For example, Seebacher et al (2005) acclimated the Antarctic notothenioid Pagothenia borchgrevinki to 4°C, a temperature likely to be 3.5°C greater than they experience in the wild.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, B. saida clearly have some capacity for thermal acclimation as do (despite the differences in evolution) Antarctic species, which experience true stenothermal conditions year round (Pörtner et al, 2000;Lannig et al, 2005;Seebacher et al, 2005;Franklin et al, 2007). Thermal acclimation likely translates into a capacity for B. saida to exploit the thermally stratified Arctic Ocean in the summer (see Fig.…”

Section: Introductionmentioning

confidence: 99%

Acclimation potential of Arctic cod (Boreogadus saida Lepechin) from the rapidly warming Arctic Ocean

Drost

Carmack

et al. 2016

Journal of Experimental Biology

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As a consequence of the growing concern about warming of the Arctic Ocean, this study quantified the thermal acclimation responses of Boreogadus saida, a key Arctic food web fish. Physiological rates for cardio-respiratory functions as well as critical maximum temperature (T c,max ) for loss of equilibrium (LOE) were measured. The transition temperatures for these events (LOE, the rate of oxygen uptake and maximum heart rate) during acute warming were used to gauge phenotypic plasticity after thermal acclimation from 0.5°C up to 6.5°C for 1 month (respiratory and T c,max measurements) and 6 months (cardiac measurements). T c,max increased significantly by 2.3°C from 14.9°C to 17.1°C with thermal acclimation, while the optimum temperature for absolute aerobic scope increased by 4.5°C over the same range of thermal acclimation. Warm acclimation reset the maximum heart rate to a statistically lower rate, but the first Arrhenius breakpoint temperature during acute warming was unchanged. The hierarchy of transition temperatures was quantified at three acclimation temperatures and was fitted inside a Fry temperature tolerance polygon to better define ecologically relevant thermal limits to performance of B. saida. We conclude that B. saida can acclimate to 6.5°C water temperatures in the laboratory. However, at this acclimation temperature 50% of the fish were unable to recover from maximum swimming at the 8.5°C test temperature and their cardio-respiratory performance started to decline at water temperatures greater than 5.4°C. Such costs in performance may limit the ecological significance of B. saida acclimation potential.

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“…In Antarctic stenothermal eelpout, increased HIF-1-DNA binding to the EPO-enhancer over the 0°C control levels occurred upon warming to 5°C, a temperature close to the upper tolerance limit but well tolerated by this species (Mark et al 2002a;Lannig et al 2005). Similarly, warming from 12 to 18°C (but not to above 20°C) stimulated enhanced HIF-1-DNA binding in the temperate eelpout (Heise et al 2006b).…”

mentioning

confidence: 89%

Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish

Heise

Estevez²,

Puntarulo³

et al. 2007

J Comp Physiol B

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Acute, short term cooling of North Sea eelpout Zoarces viviparus is associated with a reduction of tissue redox state and activation of hypoxia inducible factor (HIF-1) in the liver. The present study explores the response of HIF-1 to seasonal cold in Zoarces viviparus, and to latitudinal cold by comparing the eurythermal North Sea fish to stenothermal Antarctic eelpout (Pachycara brachycephalum). Hypoxic signalling (HIF-1 DNA binding activity) was studied in liver of summer and winter North Sea eelpout as well as of Antarctic eelpout at habitat temperature of 0°C and after long-term warming to 5°C. Biochemical parameters like tissue iron content, glutathione redox ratio, and oxidative stress indicators were analyzed to see whether the cellular redox state or reactive oxygen species formation and HIF activation in the fish correlate. HIF-1 DNA binding activity was significantly higher at cold temperature, both in the interspecific comparison, polar vs. temperate species, and when comparing winter and summer North Sea eelpout. Compared at the low acclimation temperatures (0°C for the polar and 6°C for the temperate eelpout) the polar fish showed lower levels of lipid peroxidation although the liver microsomal fraction turned out to be more susceptible to lipid radical formation. The level of radical scavenger, glutathione, was twofold higher in polar than in North Sea eelpout and also oxidised to over 50%. Under both conditions of cold exposure, latitudinal cold in the Antarctic and seasonal cold in the North Sea eelpout, the glutathione redox ratio was more oxidised when compared to the warmer condition. However, oxidative damage parameters (protein carbonyls and thiobarbituric acid reactive substances (TBARS) were elevated only during seasonal cold exposure in Z. viviparus. Obviously, Antarctic eelpout are keeping oxidative defence mechanisms high enough to avoid accumulation of oxidative damage products at low habitat temperature. The paper discusses how HIF could be instrumental in cold adaptation in fish.

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Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation

Cited by 54 publications

References 41 publications

Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems

Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems

Acclimation potential of Arctic cod (Boreogadus saida Lepechin) from the rapidly warming Arctic Ocean

Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish

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