Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut

Self Cite

The study by Gräns et al. (Gräns et al., 2014) investigated growth performance and oxygen demand at rest and during recovery from fatiguing exercise in Atlantic halibut (Hippoglossus hippoglossus) under simulated scenarios of ocean warming and acidification. The authors claim that their data, when used to evaluate the aerobic scope for exercise, do not explain temperature-dependent growth. They thus question the general use of the concept of 'oxygen and capacity limited thermal tolerance' (OCLTT) in explaining the onset of thermal limitation of fishes under field conditions (Pörtner and Knust, 2007;Pörtner and Farrell, 2008). There are important lessons to learn from this study about how, or how not, to investigate the concept of OCLTT and aerobic scope in thermal limitation.From a conceptual point of view, the term aerobic scope should not be constrained to use only with exercise. In the context of OCLTT, it makes sense to use the term aerobic scope for all routine performances that draw on aerobic energy such as growth, reproduction and steady-state swimming. The question is whether the chasing protocol imposed on a strictly benthic fish such as halibut provide suitable estimates of performance, of aerobic scope as used by growth and of climate sensitivity.Methodological issues invariably constrain what experimental data can say. In their paper, Gräns et al. routinely measured growth in active fish. In contrast, aerobic scope was determined in fish exercised to exhaustion and from differences between EPOC (excess post-exercise oxygen consumption) and resting metabolism. An over-riding difficulty with tests using exhaustive exercise is that performance itself is not properly quantified. The physiological state of the animals during steady-state growth clearly differs from that during the non-steady recovery state post-exercise. The latter is characterized by exponentially declining oxygen consumption, very low venous P O 2 (Farrell and Clutterham, 2003; Lee et al., 2003), release of catecholamines (Reid et al., 1998), acidosis and shifted metabolite concentrations, pathways and ion equilibria, all of which are non-steady state. Furthermore, the data analysis by Gräns et al. does not build on a clear functional background. Linear regressions are used for non-linear data. At normal water pH and the highest temperature, standard metabolic rate and EPOC indicate a clear decline in metabolic scope (their fig. 1), which is not picked up by the selected polynomial fit. Also, the post hoc statistics do not support a global effect of CO 2 . For EPOC, statistical significance is reached only at certain temperatures, rather than all test temperatures. Growth was depressed by CO 2 only on the cold side of the studied temperature range, matching predictions of synergistic effects at thermal extremes (Pörtner and Farrell, 2008). Thus, the overall CO 2 effect could be viewed as small and hardly discernible.In contrast to the authors' contention, the mechanisms influencing growth have not been investigated. The paper does not ...

Section: Hans-otto Pörtnermentioning

confidence: 96%

mentioning

confidence: 97%

Response to ‘How and how not to investigate the oxygen and capacity limitation of thermal tolerance (OCLTT) and aerobic scope – remarks on the article by Gräns et al.’

Jutfelt

Gräns

Jönsson

et al. 2014

Self Cite

“…It has been contended that this loss of aerobic scope coincides with apparent decreases in tissue oxygen supplies and T HF (Farrell et al, 2009;Pörtner and Farrell, 2008;Pörtner and Peck, 2010;Wang and Overgaard, 2007). However, recent reappraisals indicate that thermal limitations on aerobic scope occur at temperatures above those constraining other crucial parameters, such as fish growth, reproduction and locomotion (Clark et al, 2013;Gräns et al, 2014;Healy and Schulte, 2012). Moreover, oxygen supply may still be adequate where these parameters fail, and potentially at and above temperatures where aerobic scope fails (Gräns et al, 2014;Iftikar and Hickey, 2013).…”

Section: The Impact Of Heat Stress On Mitochondrial Bioenergeticsmentioning

confidence: 99%

“…However, recent reappraisals indicate that thermal limitations on aerobic scope occur at temperatures above those constraining other crucial parameters, such as fish growth, reproduction and locomotion (Clark et al, 2013;Gräns et al, 2014;Healy and Schulte, 2012). Moreover, oxygen supply may still be adequate where these parameters fail, and potentially at and above temperatures where aerobic scope fails (Gräns et al, 2014;Iftikar and Hickey, 2013).…”

Section: The Impact Of Heat Stress On Mitochondrial Bioenergeticsmentioning

confidence: 99%

Could thermal sensitivity of mitochondria determine species distribution in a changing climate?

Iftikar

MacDonald

Baker

et al. 2014

For many aquatic species, the upper thermal limit (T max ) and the heart failure temperature (T HF ) are only a few degrees away from the species' current environmental temperatures. While the mechanisms mediating temperature-induced heart failure (HF) remain unresolved, energy flow and/or oxygen supply disruptions to cardiac mitochondria may be impacted by heat stress. Recent work using a New Zealand wrasse (Notolabrus celidotus) found that ATP synthesis capacity of cardiac mitochondria collapses prior to T HF . However, whether this effect is limited to one species from one thermal habitat remains unknown. The present study confirmed that cardiac mitochondrial dysfunction contributes to heat stress-induced HF in two additional wrasses that occupy cold temperate (Notolabrus fucicola) and tropical (Thalassoma lunare) habitats. With exposure to heat stress, T. lunare had the least scope to maintain heart function with increasing temperature. Heat-exposed fish of all species showed elevated plasma succinate, and the heart mitochondria from the cold temperate N. fucicola showed decreased phosphorylation efficiencies (depressed respiratory control ratio, RCR), cytochrome c oxidase (CCO) flux and electron transport system (ETS) flux. In situ assays conducted across a range of temperatures using naive tissues showed depressed complex II (CII) and CCO capacity, limited ETS reserve capacities and lowered efficiencies of pyruvate uptake in T. lunare and N. celidotus. Notably, alterations of mitochondrial function were detectable at saturating oxygen levels, indicating that cardiac mitochondrial insufficiency can occur prior to HF without oxygen limitation. Our data support the view that species distribution may be related to the thermal limits of mitochondrial stability and function, which will be important as oceans continue to warm.

“…Currently, the potential synergistic effects of increased temperature and increased Ṗ CO 2 in fish have only been examined in a small number of studies (Pankhurst and Munday, 2011;Nowicki et al, 2012;Strobel et al, 2012;Enzor et al, 2013;Strobel et al, 2013a;Strobel et al, 2013b;Gräns et al, 2014). We have previously shown that increased temperature and Ṗ CO 2 levels result in a rapid increase in resting metabolic rates in several species of Antarctic fish (Enzor et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors

Enzor

Place

2014

Antarctic fish of the suborder Notothenioidei have evolved several unique adaptations to deal with subzero temperatures. However, these adaptations may come with physiological trade-offs, such as an increased susceptibility to oxidative damage. As such, the expected environmental perturbations brought on by global climate change have the potential to significantly increase the level of oxidative stress and cellular damage in these endemic fish. Previous single stressor studies of the notothenioids have shown they possess the capacity to acclimate to increased temperatures, but the cellularlevel effects remain largely unknown. Additionally, there is little information on the ability of Antarctic fish to respond to ecologically relevant environmental changes where multiple variables change concomitantly. We have examined the potential synergistic effects that increased temperature and Ṗ CO2 have on the level of protein damage in Trematomus bernacchii, Pagothenia borchgrevinki and Trematomus newnesi, and combined these measurements with changes in total enzymatic activity of catalase (CAT) and superoxide dismutase (SOD) in order to gauge tissue-specific changes in antioxidant capacity. Our findings indicate that total SOD and CAT activity levels displayed only small changes across treatments and tissues. Short-term acclimation to decreased seawater pH and increased temperature resulted in significant increases in oxidative damage. Surprisingly, despite no significant change in antioxidant capacity, cellular damage returned to near-basal levels, and significantly decreased in T. bernacchii, after long-term acclimation. Overall, these data suggest that notothenioid fish currently maintain the antioxidant capacity necessary to offset predicted future ocean conditions, but it remains unclear whether this capacity comes with physiological trade-offs.