Albin Gräns

Experimental manipulations of tissue oxygen supply do not affect warming tolerance of European perch

ABSTRACT 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 (CTmax). Hyperoxia resulted in a twofold increase in aerobic scope at the control temperature of 23°C, but this did not translate to an elevated CTmax 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 CTmax (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 CTmax of fishes. Summary: Manipulations of oxygen availability and transport capacity in European perch show that the acute upper thermal limit of fishes is not universally limited by oxygen supply.

Cardiac oxygen limitation during an acute thermal challenge in the European perch: effects of chronic environmental warming and experimental hyperoxia

Oxygen supply to the heart has been hypothesized to limit cardiac performance and whole animal acute thermal tolerance (CTmax) 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 CTmax was 2.2°C higher in Biotest compared with reference perch, the peaks in cardiac output and heart rate prior to CTmax occurred at statistically similar Pvo2 values (2.3-4.0 kPa), suggesting that cardiac failure occurred at a common critical Pvo2 threshold. Environmental hyperoxia (200% air saturation) increased Pvo2 across temperatures in reference fish, but heart rate still declined at a similar temperature. CTmax of 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 CTmax 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.

Dynamic changes in scope for heart rate and cardiac autonomic control during warm acclimation in rainbow trout

ABSTRACT Time course studies are critical for understanding regulatory mechanisms and temporal constraints in ectothermic animals acclimating to warmer temperatures. Therefore, we investigated the dynamics of heart rate and its neuro-humoral control in rainbow trout (Onchorhynchus mykiss L.) acclimating to 16°C for 39u2005days after being acutely warmed from 9°C. Resting heart rate was 39u2005beatsu2005min−1 at 9°C, and increased significantly when fish were acutely warmed to 16°C (Q10=1.9), but then declined during acclimation (Q10=1.2 at day 39), mainly due to increased cholinergic inhibition while the intrinsic heart rate and adrenergic tone were little affected. Maximum heart rate also increased with warming, although a partial modest decrease occurred during the acclimation period. Consequently, heart rate scope exhibited a complex pattern with an initial increase with acute warming, followed by a steep decline and then a subsequent increase, which was primarily explained by cholinergic inhibition of resting heart rate. Summary: The progressively decreased resting heart rate during warm acclimation in rainbow trout is primarily explained by elevated inhibitory cholinergic tone and results in a gradual increase in heart rate scope.

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

The Commentary by Portner, Bock and Mark ([Portner 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

Cardiorespiratory upregulation during seawater acclimation in rainbow trout: effects on gastrointestinal perfusion and postprandial responses

Increased gastrointestinal blood flow is essential for euryhaline fishes to maintain osmotic homeostasis during the initial phase of a transition from freshwater to seawater. However, the cardiorespiratory responses and hemodynamic changes required for a successful long-term transition to seawater remain largely unknown. In the present study, we simultaneously measured oxygen consumption rate (ṀO2), cardiac output (CO), heart rate (HR), and gastrointestinal blood flow (GBF) in rainbow trout (Oncorhynchus mykiss) acclimated to either freshwater or seawater for at least 6 wk. Seawater-acclimated trout displayed significantly elevated ṀO2 (day: 18%, night: 19%), CO (day: 22%, night: 48%), and GBF (day: 96%, night: 147%), demonstrating that an overall cardiorespiratory upregulation occurs during seawater acclimation. The elevated GBF was achieved via a combination of increased CO, mediated through elevated stroke volume (SV), and a redistribution of blood flow to the gastrointestinal tract. Interestingly, virtually all of the increase in CO of seawater-acclimated trout was directed to the gastrointestinal tract. Although unfed seawater-acclimated trout displayed substantially elevated cardiorespiratory activity, the ingestion of a meal resulted in a similar specific dynamic action (SDA) and postprandial GBF response as in freshwater-acclimated fish. This indicates that the capacity for the transportation of absorbed nutrients, gastrointestinal tissue oxygen delivery, and acid-base regulation is maintained during digestion in seawater. The novel findings presented in this study clearly demonstrate that euryhaline fish upregulate cardiovascular function when in seawater, while retaining sufficient capacity for the metabolic and cardiovascular changes associated with the postprandial response.

Influence of the coronary circulation on thermal tolerance and cardiac performance during warming in rainbow trout

Thermal tolerance in fish may be related to an oxygen limitation of cardiac function. While the hearts of some fish species receive oxygenated blood via a coronary circulation, the influence of this oxygen supply on thermal tolerance and cardiac performance during warming remain unexplored. Here, we analyzed the effect in vivo of acute warming on coronary blood flow in adult sexually mature rainbow trout (Onchorhynchus mykiss) and the consequences of chronic coronary ligation on cardiac function and thermal tolerance in juvenile trout. Coronary blood flow at 10°C was higher in females than males (0.56 ± 0.08 vs. 0.30 ± 0.08 ml·min-1·g ventricle-1), and averaged 0.47 ± 0.07 ml·min-1·g ventricle-1 across sexes. Warming increased coronary flow in both sexes until 14°C, at which it peaked and plateaued at 0.78 ± 0.1 and 0.61 ± 0.1 ml·min-1·g ventricle-1 in females and males, respectively. Thus, the scope for increasing coronary flow was 101% in males, but only 39% in females. Coronary-ligated juvenile trout exhibited elevated heart rate across temperatures, reduced Arrhenius breakpoint temperature for heart rate (23.0 vs. 24.6°C), and reduced upper critical thermal maximum (25.3 vs. 26.3°C). To further analyze the effects of coronary flow restriction on cardiac rhythmicity, electrocardiogram characteristics were determined before and after coronary occlusion in anesthetized trout. Occlusion resulted in reduced R-wave amplitude and an elevated S-T segment, indicating myocardial ischemia, while heart rate was unaffected. This suggests that the tachycardia in ligated trout across temperatures in vivo was mainly to compensate for reduced cardiac contractility to maintain cardiac output. Moreover, our findings show that coronary flow increases with warming in a sex-specific manner. This may improve whole animal thermal tolerance, presumably by sustaining cardiac oxygenation and contractility at high temperatures.

Stunning fish with CO2 or electricity: contradictory results on behavioural and physiological stress responses.

Studies that address fish welfare before slaughter have concluded that many of the traditional systems used to stun fish including CO2 narcosis are unacceptable as they cause avoidable stress before death. One system recommended as a better alternative is electrical stunning, however, the welfare aspects of this method are not yet fully understood. To assess welfare in aquaculture both behavioural and physiological measurements have been used, but few studies have examined the relationship between these variables. In an on-site study aversive behaviours and several physiological stress indicators, including plasma levels of cortisol and ions as well as blood physiological variables, were compared in Arctic char (Salvelinus alpinus) stunned with CO2 or electricity. Exposure to water saturated with CO2 triggered aversive struggling and escape responses for several minutes before immobilization, whereas in fish exposed to an electric current immobilization was close to instant. On average, it took 5 min for the fish to recover from electrical stunning, whereas fish stunned with CO2 did not recover. Despite this, the electrically stunned fish had more than double the plasma levels of cortisol compared with fish stunned with CO2. This result is surprising considering that the behavioural reactions were much more pronounced following CO2 exposure. These contradictory results are discussed with regard to animal welfare and stress physiological responses. The present results emphasise the importance of using an integrative and interdisciplinary approach and to include both behavioural and physiological stress indicators in order to make accurate welfare assessments of fish in aquaculture.

Cardiac reflexes in a warming world: thermal plasticity of barostatic control and autonomic tones in a temperate fish

ABSTRACT Thermal plasticity of cardiorespiratory function allows ectotherms like fish to cope with seasonal temperature changes and is critical for resilience to climate change. Yet, the chronic thermal effects on cardiovascular homeostatic reflexes in fish are little understood although this may have important implications for physiological performance and overall resilience to climate warming. We compared cardiac autonomic control and baroreflex regulation of heart rate in perch (Perca fluviatilis L.) from a reference area in the Baltic Sea at 18–19°C with conspecifics from the Biotest enclosure, a chronically heated ecosystem receiving warmed effluent water (24–25°C) from a nuclear power plant. Resting heart rate of Biotest fish displayed clear thermal compensation and was 58.3±2.3 beats min−1 compared with 52.4±2.6 beats min−1 in reference fish at their respective environmental temperatures (Q10=1.2). The thermally compensated heart rate of Biotest fish was a combined effect of elevated inhibitory cholinergic tone (105% in Biotest fish versus 70% in reference fish) and reduced intrinsic cardiac pacemaker rate. A barostatic response was evident in both groups, as pharmacologically induced increases and decreases in blood pressure resulted in atropine-sensitive bradycardia and tachycardia, respectively. Yet, the tachycardia in Biotest fish was significantly greater, presumably due to the larger scope for vagal release. Acclimation of Biotest fish to 18°C for 3u2005weeks abolished differences in intrinsic heart rate and autonomic tone, suggesting considerable short-term thermal plasticity of cardiovascular control in this species. The heightened hypotensive tachycardia in Biotest perch may represent an important mechanism of ectothermic vertebrates that safeguards tissue perfusion pressure when tissue oxygen demand is elevated by environmental warming. Summary: Perch from a chronically warmed ecosystem exhibit profound thermal compensation of resting heart rate through increased cholinergic tone and heightened baroreflex sensitivity; the latter may safeguard tissue perfusion pressure when tissue oxygen demand is elevated by environmental warming.

In vivo aerobic metabolism of the rainbow trout gut and the effects of an acute temperature increase and stress event

ABSTRACT The fish gut is responsible for numerous potentially energetically costly processes, yet little is known about its metabolism. Here, we provide the first in vivo measurements of aerobic metabolism of the gut in a teleost fish by measuring gut blood flow, as well as arterial and portal venous oxygen content. At 10°C, gut oxygen uptake rate was 4.3±0.5u2005mlu2005O2 h−1 kg−1 (∼11% of whole-animal oxygen uptake). Following acute warming to 15°C, gut blood flow increased ∼3.4-fold and gut oxygen uptake rate increased ∼3.7-fold (16.0±3.3u2005mlu2005O2 h−1 kg−1), now representing ∼25% of whole-animal oxygen uptake. Although gut blood flow decreased following an acute stress event at 15°C, gut oxygen uptake remained unchanged as a result of a ∼2-fold increase in oxygen extraction. The high metabolic thermal sensitivity of the gut could have important implications for the overall aerobic capacity and performance of fish in a warming world and warrants further investigation. Summary: In vivo recordings of gut oxygen uptake in a teleost fish demonstrate a high metabolic sensitivity to an acute temperature increase, as well as the metabolic responses to stress.

Effects of coeliacomesenteric blood flow reduction on intestinal barrier function in rainbow trout Oncorhynchus mykiss

The aim of the current work was to elucidate if there is a connection between stress-induced decrease in coeliacomesenteric artery blood flow (i.e. gastrointestinal blood flow; GBF) and disruption of the intestinal primary barrier in rainbow trout Oncorhynchus mykiss. Upon initiation of a 15 min acute chasing stress, the GBF decreased instantly by c. 92%. The GBF then slowly increased and reached c. 28% of resting values at the end of the stress protocol. After the stress was ceased, the GBF slowly increased and returned to resting values within c. 45 min. Intestinal permeability assessment in an Ussing-chambers set-up revealed impaired intestinal barrier function 24 h after stress. When the stress-induced GBF reduction was mimicked by an experimental occlusion of the coeliacomesenteric artery for 15 min followed by 24 h recovery, no effect on intestinal barrier function was observed. These results suggest that no direct causal relationship can be found between the GBF reduction and development of intestinal barrier dysfunction following periods of acute stress in this species of fish.