Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology

Jutfelt, Fredrik; Norin, Tommy; Ern, Rasmus; Overgaard, Johannes; Wang, Tobias; McKenzie, David J.; Lefevre, Sjannie; Nilsson, Göran; Metcalfe, Neil B.; Hickey, Anthony J. R.; Brijs, Jeroen; Speers‐Roesch, Ben; Roche, Dominique G.; Gamperl, A. Kurt; Raby, Graham D.; Morgan, Rachael; Esbaugh, Andrew J.; Gräns, Albin; Axelsson, Michael; Ekström, Andreas; Sandblom, Erik; Binning, Sandra A.; Hicks, James W.; Seebacher, Frank; Jørgensen, Christian; Killen, Shaun S.; Schulte, Patricia M.; Clark, Timothy D.

doi:10.1242/jeb.169615

Cited by 218 publications

(142 citation statements)

References 22 publications

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“…Our results support this prediction, as warm-habitat sticklebacks tended to have a lower AS than cold-habitat sticklebacks at a high temperature (20 o C). It has been proposed that the capacity to meet increased oxygen demands at elevated temperatures may determine the persistence of fish populations in a warming climate (Donelson et al 2011; but see Lefevre 2016, Jutfelt et al 2018, so it is important to better understand and predict changes in AS in response to temperature changes (Sinclair et al 2016).…”

Section: Discussionmentioning

confidence: 99%

“…AS has therefore been suggested to play a key role in the response of fish populations to changing temperatures (Farrell 2016, Sandblom et al 2016. Notably, however, many fish species appear to show little or no change in AS with changes in temperature (Lefevre 2016, Nati et al 2016, Jutfelt et al 2018, so the degree to which AS limits adaptive responses to warming remains an open question.…”

Section: Introductionmentioning

confidence: 99%

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Multigenerational exposure to elevated temperatures leads to a reduction in standard metabolic rate in the wild

Pilakouta

Killen

Kristjánsson

et al. 2019

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1. In light of global climate change, there is a pressing need to understand and predict the capacity of populations to respond to rising temperatures. Metabolic rate is a key trait that is likely to influence the ability to cope with climate change. Yet, empirical and theoretical work on metabolic rate responses to temperature changes has so far produced mixed results and conflicting predictions.2. Our study addresses this issue using a novel approach of comparing fish populations in geothermally warmed lakes and adjacent ambient-temperature lakes in Iceland. This unique 'natural experiment' provides repeated and independent examples of populationsexperiencing contrasting thermal environments for many generations over a small geographic scale, thereby avoiding the confounding factors associated with latitudinal or elevational comparisons. Using Icelandic sticklebacks from three warm and three cold habitats, we measured individual metabolic rates across a range of acclimation temperatures to obtain reaction norms for each population.3. We found a general pattern for a lower standard metabolic rate in sticklebacks from warm habitats when measured at a common temperature, as predicted by Krogh's rule.Metabolic rate differences between warm-and cold-habitat sticklebacks were more pronounced at more extreme acclimation temperatures, suggesting the release of cryptic genetic variation upon exposure to novel conditions, which can reveal hidden evolutionary potential. We also found a stronger divergence in metabolic rate between thermal habitats in allopatry than sympatry, indicating that gene flow may constrain physiological adaptation when dispersal between warm and cold habitats is possible. 3 4. In sum, our study suggests that fish may diverge toward a lower standard metabolic rate in a warming world, but this might depend on connectivity and gene flow between different thermal habitats.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Multigenerational exposure to elevated temperatures leads to a reduction in standard metabolic rate in the wild

Pilakouta

Killen

Kristjánsson

et al. 2019

Preprint

Self Cite

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“…When warming pushes an animal’s metabolic rate to levels where oxygen delivery is insufficient, tissue hypoxia ensues (Pörtner and Knust, 2007). The OCLTT hypothesis remains controversial, yet can be used to form testable predictions (Clark et al, 2013; Jutfelt et al, 2018). Accordingly, OCLTT predicts that brain hypoxia would cause LOE during heat challenges.…”

Section: Resultsmentioning

confidence: 99%

Brain cooling marginally increases maximum thermal tolerance in Atlantic cod

Jutfelt

Norin

et al. 2019

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25 tolerance (OCLTT), critical thermal maximum (CT max ), loss of equilibrium (LOE), thermal 26 ramping 27 2 28 Summary statement 29We tested whether brain temperature sets the upper thermal limit in a fish. Selectively cooling 30 the brain during whole-organism thermal ramping marginally increased thermal tolerance. 31 32 ABSTRACT 33 The physiological mechanisms determining thermal limits in fishes are debated but remain 34 elusive. It has been hypothesised that loss of motor function observed as a loss of equilibrium 35 during an acute thermal challenge is due to direct thermal effects on brain neuronal function. 36To test this hypothesis, we mounted cooling plates on the head of Atlantic cod (Gadus 37 morhua) and quantified whether local cooling of the brain increased whole-organism critical 38 thermal maxima (CT max ). Brain cooling reduced brain temperature by 2-6°C and increased 39 CT max by 0.5-0.7°C relative to instrumented and uninstrumented controls, suggesting that 40 direct thermal effects on brain neurons might contribute to setting upper thermal limits in fish. 41However, the improvement in CT max with brain cooling was small relative to the difference in 42 brain temperature, demonstrating that other mechanisms (e.g., failure of spinal and peripheral 43 neurons, or muscle) may also contribute to controlling acute thermal tolerance in fishes. 44 45

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“…Thermal preferences can shift with environmental conditions along distinct spatial gradients, thereby challenging the ability of organisms to exploit local environmental heterogeneity to evade stressful environments. For example, any animals facing climate warming sometimes shift geographic ranges to higher altitudes, but in so doing expose themselves to reduced oxygen levels, which can compromise physiological performance and even reduce heat tolerance in some species (Jutfelt et al 2018;Pörtner et al 2017Pörtner et al , 2018, including embryonic reptiles (Liang et al 2015;Smith et al 2015).…”

Section: Heterogeneity and Behavioral Evasionmentioning

confidence: 99%

“…Williams et al (2018) provide an exemplar exploration of the physiological mechanisms and costs of genetic adaptation to low body temperatures. At issue is whether oxygen limitation affects energy supplies (Pörtner et al 2017(Pörtner et al , 2018Jutfelt et al 2018). Using evolutionary lines of Drosophila artificially selected for fast versus slow recovery from a cold exposure ("chill coma"), they investigate whether adaptation to cold involves physiological changes to maintain ATP homeostasis.…”

Section: Evolutionary Adjustmentsmentioning

confidence: 99%