Understanding the resilience of aquatic ectothermic animals to climate warming has been hindered by the absence of experimental systems experiencing warming across relevant timescales (for example, decades). Here, we examine European perch (Perca fluviatilis, L.) from the Biotest enclosure, a unique coastal ecosystem that maintains natural thermal fluctuations but has been warmed by 5–10 °C by a nuclear power plant for over three decades. We show that Biotest perch grow faster and display thermally compensated resting cardiorespiratory functions compared with reference perch living at natural temperatures in adjacent waters. However, maximum cardiorespiratory capacities and heat tolerance limits exhibit limited or no thermal compensation when compared with acutely heated reference perch. We propose that while basal energy requirements and resting cardiorespiratory functions (floors) are thermally plastic, maximum capacities and upper critical heat limits (ceilings) are much less flexible and thus will limit the adaptive capacity of fishes in a warming climate.

The Commentary by Pörtner, Bock and Mark ([Pörtner et al., 2017][1]) elaborates on the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Journal of Experimental Biology Commentaries allow for personal and controversial views, yet the journal also mandates that ‘opinion and fact

Oxygen supply to the heart has been hypothesized to limit cardiac performance and whole animal acute thermal tolerance (CT_max) in fish. We tested these hypotheses by continuously measuring venous oxygen tension (Pvo₂) and cardiovascular variables in vivo during acute warming in European perch ( Perca fluviatilis) from a reference area during summer (18°C) and a chronically heated area (Biotest enclosure) that receives warm effluent water from a nuclear power plant and is normally 5–10°C above ambient (24°C at the time of experiments). While CT_maxwas 2.2°C higher in Biotest compared with reference perch, the peaks in cardiac output and heart rate prior to CT_maxoccurred at statistically similar Pvo₂values (2.3–4.0 kPa), suggesting that cardiac failure occurred at a common critical Pvo₂threshold. Environmental hyperoxia (200% air saturation) increased Pvo₂across temperatures in reference fish, but heart rate still declined at a similar temperature. CT_maxof reference fish increased slightly (by 0.9°C) in hyperoxia, but remained significantly lower than in Biotest fish despite an improved cardiac output due to an elevated stroke volume. Thus, while cardiac oxygen supply appears critical to elevate stroke volume at high temperatures, oxygen limitation may not explain the bradycardia and arrhythmia that occur prior to CT_max. Acute thermal tolerance and its thermal plasticity can, therefore, only be partially attributed to cardiac failure from myocardial oxygen limitations, and likely involves limiting factors on multiple organizational levels.

Cellular and mitochondrial metabolic capacity of the heart has been suggested to limit performance of fish at warm temperatures. We investigated this hypothesis by studying the effects of acute temperature increases (16, 23, 30, 32.5 and 36°C) on the thermal sensitivity of 10 key enzymes governing cardiac oxidative and glycolytic metabolism in two populations of European perch (Perca fluviatilis) field-acclimated to 15.5 and 22.5°C, as well as the effects of acclimation on cardiac lipid composition. In both populations of perch, the activity of glycolytic (pyruvate kinase and lactate dehydrogenase) and tricarboxylic acid cycle (pyruvate dehydrogenase and citrate synthase) enzymes increased with acute warming. However, at temperatures exceeding 30°C, a drastic thermally-induced decline in citrate synthase activity was observed in the cold- and warm-acclimated populations respectively, indicating a bottleneck for producing the reducing equivalents required for oxidative phosphorylation. Yet, the increase in aspartate aminotransferase and malate dehydrogenase activities occurring in both populations at temperatures exceeding 30°C, suggests that the malate-aspartate shuttle may aid to maintain cardiac oxidative capacities at high temperatures. Warm acclimation resulted in a reorganization of the lipid profile, a general depression of enzymatic activity and an increased fatty acid metabolism and oxidative capacity. While these compensatory mechanisms may contribute to maintain cardiac energy production at high temperatures, the activity of the electron transport system enzymes, such as complexes I and IV, declined at 36°C in both populations indicating a thermal limit of oxidative phosphorylation capacity in the heart of European perch.

A progressive inability of the cardiorespiratory system to maintain systemic oxygen supply at elevated temperatures has been suggested to reduce aerobic scope and the upper thermal limit of aquatic ectotherms. However, few studies have directly investigated the dependence of thermal limits on oxygen transport capacity. By manipulating oxygen availability (via environmental hyperoxia) and blood oxygen carrying capacity (via experimentally induced anaemia) in European perch (Perca fluviatilis Linneaus), we investigated the effects of oxygen transport capacity on aerobic scope and the critical thermal maximum (CT_max). Hyperoxia resulted in a twofold increase in aerobic scope at the control temperature of 23°C, but this did not translate to an elevated CT_max in comparison with control fish (34.6±0.1 versus 34.0±0.5°C, respectively). Anaemia (∼43% reduction in haemoglobin concentration) did not cause a reduction in aerobic scope or CT_max (33.8±0.3°C) compared with control fish. Additionally, oxygen consumption rates of anaemic perch during thermal ramping increased in a similar exponential manner to that in control fish, highlighting that perch have an impressive capacity to compensate for a substantial reduction in blood oxygen carrying capacity. Taken together, these results indicate that oxygen limitation is not a universal mechanism determining the CT_max of fishes.