Cardiac Thermal Tolerance Research Articles

Body size and temperature affect metabolic and cardiac thermal tolerance in fish

Environmental warming is associated with reductions in ectotherm body sizes, suggesting that larger individuals may be more vulnerable to climate change. The mechanisms driving size-specific vulnerability to temperature are unknown but are required to finetune predictions of fisheries productivity and size-structure community responses to climate change. We explored the potential metabolic and cardiac mechanisms underlying these body size vulnerability trends in a eurythermal fish, barred surfperch. We acutely exposed surfperch across a large size range (5–700 g) to four ecologically relevant temperatures (16 °C, 12 °C, 20 °C, and 22 °C) and subsequently, measured their metabolic capacity (absolute and factorial aerobic scopes, maximum and resting metabolic rates; AAS, FAS, MMR, RMR). Additionally, we estimated the fish’s cardiac thermal tolerance by measuring their maximum heart rates (fHmax) across acutely increasing temperatures. Barred surfperch had parallel hypoallometric scaling of MMR and RMR (exponent 0.81) and a weaker hypoallometric scaling of fHmax (exponent − 0.05) across all test temperatures. In contrast to our predictions, the fish’s aerobic capacity was maintained across sizes and acute temperatures, and larger fish had greater cardiac thermal tolerance than smaller fish. These results demonstrate that thermal performance may be limited by different physiological constraints depending on the size of the animal and species of interest.

Mechanisms of cardiac collapse at high temperature in a marine teleost (Girella nigrians)

Heat-induced mortality in ectotherms may be attributed to impaired cardiac performance, specifically a collapse in maximum heart rate (fHmax), although the physiological mechanisms driving this phenomenon are still unknown. Here, we tested two proposed factors which may restrict cardiac upper thermal limits: noxious venous blood conditions and oxygen limitation. We hypothesized elevated blood [K+] (hyperkalemia) and low oxygen (hypoxia) would reduce cardiac upper thermal limits in a marine teleost (Girella nigricans), while high oxygen (hyperoxia) would increase thermal limits. We also hypothesized higher acclimation temperatures would exacerbate the harmful effects of an oxygen limitation. Using the Arrhenius breakpoint temperature test, we measured fHmax in acutely warmed fish under control (saline injected) and hyperkalemic conditions (elevated plasma [K+]) while exposed to hyperoxia (200% air saturation), normoxia (100% air saturation), or hypoxia (20% air saturation). We also measured ventricle lactate content and venous blood oxygen partial pressure (PO2) to determine if there were universal thresholds in either metric driving cardiac collapse. Elevated [K+] was not significantly correlated with any cardiac thermal tolerance metric. Hypoxia significantly reduced cardiac upper thermal limits (Arrhenius breakpoint temperature [TAB], peak fHmax, temperature of peak heart rate [TPeak], and temperature at arrhythmia [TARR]). Hyperoxia did not alter cardiac thermal limits compared to normoxia. There was no evidence of a species-wide threshold in ventricular [lactate] or venous PO2. Here, we demonstrate that oxygen limits cardiac thermal tolerance only in instances of hypoxia, but that other physiological processes are responsible for causing temperature-induced heart failure when oxygen is not limited.

Cardiac performance and heat shock response variation related to shell colour morphs in the mudflat snail Batillaria attramentaria.

Gastropods exhibit remarkable variation in shell colour within and among populations, but the function of shell colour is often not clear. In the present study, body temperature in the field and physiological and transcriptomic responses to thermal stress were investigated in different shell colour morphs of the mudflat snail Batillaria attramentaria. Using biomimetic models, we found that the body temperature of snails with a dark unbanded shell (D-type morph) was slightly higher than that of snails with a white line on the upper side of each whorl (UL-type morph) when exposed to sunlight. Despite no differences in upper lethal temperature among shell colour morphs, their Arrhenius breakpoint temperature (ABT) for cardiac thermal performance differed significantly, and the ABT of snails with the D-type morph was higher than that of snails with the UL-type morph. Transcriptomic analysis showed that D-type snails exhibit higher levels of four heat shock proteins (HSPs) than UL-type snails at control temperature. The unfolded protein response was activated in UL-type snails but not in D-type snails under moderate thermal stress. And 11 HSPs showed an increase in UL-type snails in contrast to 1 HSP in D-type snails, suggesting a 'preparative defence' strategy of the heat shock response in D-type snails under moderate thermal stress. When exposed to sublethal temperature, eight molecular chaperones were uniquely upregulated in D-type snails, suggesting these genes may allow D-type snails to improve their cardiac thermal tolerance. Our results suggest that the preparative defence strategies and higher ABT for cardiac thermal performance may allow the dark shell snails to adapt to rapid and stronger thermal stress in the field.

Warm, but not hypoxic acclimation, prolongs ventricular diastole and decreases the protein level of Na+/Ca2+ exchanger to enhance cardiac thermal tolerance in European sea bass

One of the physiological mechanisms that can limit the fish's ability to face hypoxia or elevated temperature, is maximal cardiac performance. Yet, few studies have measured how cardiac electrical activity and associated calcium cycling proteins change with acclimation to those environmental stressors. To examine this, we acclimated European sea bass for 6 weeks to three experimental conditions: a seasonal average temperature in normoxia (16 °C; 100% air sat.), an elevated temperature in normoxia (25 °C; 100% air sat.) and a seasonal average temperature in hypoxia (16 °C; 50% air sat.). Following each acclimation, the electrocardiogram was measured to assess how acclimation affected the different phases of cardiac cycle, the maximal heart rate (fHmax) and cardiac thermal performance during an acute increase of temperature. Whereas warm acclimation prolonged especially the diastolic phase of the ventricular contraction, reduced the fHmax and increased the cardiac arrhythmia temperature (TARR), hypoxic acclimation was without effect on these functional indices. We measured the level of two key proteins involved with cellular relaxation of cardiomyocytes, i.e. sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA) and Na+/Ca2+ exchanger (NCX). Warm acclimation reduced protein level of both NCX and SERCA and hypoxic acclimation reduced SERCA protein levels without affecting NCX. The changes in ventricular NCX level correlated with the observed changes in diastole duration and fHmax as well as TARR. Our results shed new light on mechanisms of cardiac plasticity to environmental stressors and suggest that NCX might be involved with the observed functional changes, yet future studies should also measure its electrophysiological activity.

Aerobic Exercise Training With Optimal Intensity Increases Cardiac Thermal Tolerance in Juvenile Rainbow Trout

Domestication and selective breeding for rapid-growth have impaired the cardiorespiratory system of salmonids, which might compromise their capacity to tolerate environmental stressors, such as heat waves. Exercise training by swimming has been proposed as a potential tool to enhance growth, cardiac function and disease resilience in farmed fish and thereby improves aquaculture production. However, whether exercise training could also improve cardiac robustness against heat waves, which are becoming more common and cause severe challenges to aquaculture, remains unknown. Here, we trained juvenile rainbow trout at three different training velocities: 0.06 m*s-1 (or 0.9 body lengths per second [bl*s-1]; control group), 0.11 m*s-1 (or 1.7 bl*s-1; medium speed group) and 0.17 m*s-1 (or 2.7 bl*s-1; high speed group) for 5 weeks, 6h per day, 5 days per week. Measuring maximal heart rate (fHmax) during acute warming, we demonstrated that training at 1.7 bl*s-1 was optimal in order to increase the temperature at which fHmax reached its peak (Tpeak) as well as the upper thermal tolerance of the cardiovascular function (arrhythmia temperature, TARR), up to 3.6°C as compared to the control fish. However, more intensive training did not provide similar improvement on thermal tolerance. Both training regimes enhanced the ventricular citrate synthase activity which may provide higher aerobic energy production capacity for ventricles. Further mechanistic studies are needed to understand the complex interactions between training intensities and changes in thermal tolerance. Although not conclusive on that point, our findings present a valid training programme for hatchery salmonids to increase their cardiac thermal tolerance and consequently probably also their capacity to tolerate heat waves, which has a direct application for aquaculture.

The interactive effects of exercise training and functional feeds on the cardiovascular performance of rainbow trout (Oncorhynchus mykiss) at high temperatures.

The cardiovascular performance of salmonids in aquaculture can be impaired by acute climate warming, posing risks for fish survival. Exercise training and functional feeds have been shown to be cardioprotective in mammals but their action on the fish heart and its upper thermal performance has not been studied. To investigate this, rainbow trout were trained at a moderate water velocity of 1 body length per second (bl s−1) for 6 h per day, either alone or in combination with one of two functional feed-supplements, allicin and fucoidan. After 6 weeks of exercise training and feeding, maximum heart rate and the temperature coefficient of heart rate were significantly higher in the trained fish as compared to untrained ones. There was a slight increase in hematocrit in trained control fish reared on a normal diet (TC group) compared to untrained fish fed with the same diet (CC). This implies that exercise training enhanced oxygen delivery to trout tissues via an increase of cardiac blood flow in warm water. However, cardiac thermal tolerance was not affected by exercise training or feeding, except from the temperature of peak heart rate which was higher in the trained group fed with fucoidan supplement (TF) as compared to the untrained group fed with same diet (CF). Allicin supplement caused a significant reduction in the maximum heart rate and the temperature coefficient of heart rate, especially in trained fish, while fucoidan supplement did not cause any effect on heart rate. No differences were observed in growth performance among groups. However, fish fed with fucoidan-supplemented diet had a slight reduction in feed conversion efficiency. We suggest further investigations to understand the antagonistic effect of allicin supplemental feeding and exercise training on cardiovascular performance. More studies are also required to investigate if other exercise training intensities could increase cardiac thermal tolerance.

Diet mediates thermal performance traits: implications for marine ectotherms

Thermal acclimation is a key process enabling ectotherms to cope with temperature change. To undergo a successful acclimation response, ectotherms require energy and nutritional building blocks obtained from their diet. However, diet is often overlooked as a factor that can alter acclimation responses. Using a temperate omnivorous fish, opaleye (Girella nigricans), as a model system, we tested the hypotheses that (1) diet can impact the magnitude of thermal acclimation responses and (2) traits vary in their sensitivity to both temperature acclimation and diet. We fed opaleye a simple omnivorous diet (ad libitum Artemia sp. and Ulva sp.) or a carnivorous diet (ad libitum Artemia sp.) at two ecologically relevant temperatures (12 and 20°C) and measured a suite of whole-animal (growth, sprint speed, metabolism), organ (cardiac thermal tolerance) and cellular-level traits (oxidative stress, glycolytic capacity). When opaleye were offered two diet options compared with one, they had reduced cardiovascular thermal performance and higher standard metabolic rate under conditions representative of the maximal seasonal temperature the population experiences (20°C). Further, sprint speed and absolute aerobic scope were insensitive to diet and temperature, while growth was highly sensitive to temperature but not diet, and standard metabolic rate and maximum heart rate were sensitive to both diet and temperature. Our results reveal that diet influences thermal performance in trait-specific ways, which could create diet trade-offs for generalist ectotherms living in thermally variable environments. Ectotherms that alter their diet may be able to regulate their performance at different environmental temperatures.

The thermal acclimation potential of maximum heart rate and cardiac heat tolerance in Arctic char (Salvelinus alpinus), a northern cold-water specialist.

Increasing heart rate (ƒH) is a central, if not primary mechanism used by fishes to support their elevated tissue oxygen consumption during acute warming. Thermal acclimation can adjust this acute response to improve cardiac performance and heat tolerance under the prevailing temperatures. We predict that such acclimation will be particularly important in regions undergoing rapid environmental change such as the Arctic. Therefore, we acclimated Arctic char (Salvelinus alpinus), a high latitude, cold-adapted salmonid, to ecologically relevant temperatures (2, 6, 10, 14 and 18°C) and examined how thermal acclimation influenced their cardiac heat tolerance by measuring the maximum heart rate (ƒHmax) response to acute warming. As expected, acute warming increased ƒHmax in all Arctic char before ƒHmax reached a peak and then became arrhythmic. The peak ƒHmax, and the temperature at which peak ƒHmax (Tpeak) and that at which arrhythmia first occurred (Tarr) all increased progressively (+33%, 49% and 35%, respectively) with acclimation temperature from 2 to 14°C. When compared at the same test temperature ƒHmax also decreased by as much as 29% with increasing acclimation temperature, indicating significant thermal compensation. The upper temperature at which fish first lost their equilibrium (critical thermal maximum: CTmax) also increased with acclimation temperature, albeit to a lesser extent (+11%). Importantly, Arctic char experienced mortality after several weeks of acclimation at 18°C and survivors did not have elevated cardiac thermal tolerance. Collectively, these findings suggest that if wild Arctic char have access to suitable temperatures (<18°C) for a sufficient duration, warm acclimation can potentially mitigate some of the cardiorespiratory impairments previously documented during acute heat exposure.

Plasticity of foot muscle and cardiac thermal limits in the limpet Lottia limatula from locations with differing temperatures

AB Aquatic Biology Contact the journal Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections AB 28:113-125 (2019) - DOI: https://doi.org/10.3354/ab00714 Plasticity of foot muscle and cardiac thermal limits in the limpet Lottia limatula from locations with differing temperatures Terrance Wang1,*, Richelle L. Tanner1,2, Eric J. Armstrong1,2, David R. Lindberg1,3, Jonathon H. Stillman1,2 1Department of Integrative Biology, University of California, 3040 Valley Life Sciences Building #3140, Berkeley, CA 94720-3140, USA 2Estuary & Ocean Science Center and Department of Biology, Romberg Tiburon Campus, San Francisco State University, 3150 Paradise Drive, Tiburon, CA 94920, USA 3Museum of Paleontology, University of California, 1101 Valley Life Sciences Building, Berkeley, CA 94720-4780, USA *Corresponding author: twangs@berkeley.edu ABSTRACT: Species distributions are shifting in response to increased habitat temperatures as a result of ongoing climate change. Understanding variation in physiological plasticity among species and populations is important for predicting these distribution shifts. Interspecific variation in intertidal ectotherms’ short-term thermal plasticity has been well established. However, intraspecific variation among populations from differing thermal habitats remains a question pertinent to understanding the effects of climate change on species’ ranges. In this study, we explored upper thermal tolerance limits and plasticity of those limits using a foot muscle metric and 2 cardiac metrics (Arrhenius breakpoint temperature, ABT, and flatline temperature, FLT) in adult file limpets Lottia limatula. Limpets were collected from thermally different coastal and inland-estuarine habitats and held for 2 wk at 13, 17 or 21°C prior to thermal performance assays. Compared to limpets from the warm estuary site, limpets from the cold outer coast site had similar foot muscle critical thermal maxima (CTmax; 35.2 vs. 35.6°C) but lower cardiac thermal tolerances (ABT: 30.5 vs. 35.1°C). Limpets from the cold coast site had higher acclimation responses in foot muscle CTmax (0.22°C per 1°C rise in acclimation) than those of the warm estuary site (0.07°C per 1°C rise in acclimation), but lower acclimation responses in cardiac thermal tolerance (ABT: -0.85°C per 1°C rise in acclimation) than those of the estuary site (ABT: 0.10°C per 1°C rise in acclimation). Since outer coast populations had lower cardiac plasticity and higher mortalities in the warm acclimation, we predict L. limatula from colder habitats will be more susceptible to rising temperatures. Our findings illustrate the importance of population-specific variation in short-term thermal plasticity when considering the effects of climate change on ectotherms. KEY WORDS: Intertidal · Ectotherm · Thermal tolerance · Plasticity · Acclimation · Ecophysiology Full text in pdf format Supplementary material PreviousNextCite this article as: Wang T, Tanner RL, Armstrong EJ, Lindberg DR, Stillman JH (2019) Plasticity of foot muscle and cardiac thermal limits in the limpet Lottia limatula from locations with differing temperatures. Aquat Biol 28:113-125. https://doi.org/10.3354/ab00714 Export citation Mail this link - Contents Mailing Lists - RSS Facebook - Tweet - linkedIn Cited by Published in AB Vol. 28. Online publication date: September 19, 2019 Print ISSN: 1864-7782; Online ISSN: 1864-7790 Copyright © 2019 Inter-Research.

Impact of heating rate on cardiac thermal tolerance in the California mussel, Mytilus californianus.

Intertidal communities of wave-swept rocky shores have served as a powerful model system for experiments in ecology, and mussels (the dominant competitor for space in the mid-intertidal zone) play a central role in determining community structure in this physically stressful habitat. Consequently, the ability to account for mussels' physiological responses to thermal stress affects ecologists' capacity to predict the impacts of a warming climate on this ecosystem. Here, we examined the effect of heating rate on cardiac thermal tolerance in the ribbed mussel, Mytilus californianus, comparing populations from high and low sites in the intertidal zone where emersion duration leads to different mean daily heating rates. Two temperature-related cardiac variables were examined: (1) the critical temperature (Tcrit) at which heart rate (HR) precipitously declines, and (2) flatline temperature (FLT) where HR reaches zero. Mussels were heated in air at slow, moderate and fast rates, and HR was measured via an infrared sensor affixed to the shell. Faster heating rates significantly increased Tcrit in high- but not low-zone mussels, and Tcrit was higher in high- versus low-zone mussels, especially at the fastest heating rate. By contrast, FLT did not differ between zones, and was minimally affected by heating rate. As heating rate significantly impacted high- but not low-zone mussels' cardiac thermal tolerance, realistic zone-specific heating rates must be used in laboratory tests if those tests are to provide accurate information for ecological models attempting to predict the effects of increasing temperature on intertidal communities.

Variations in cardiac performance and heat shock protein expression to thermal stress in two differently zoned limpets on a tropical rocky shore

Understanding variation in physiological adaptations to thermal stress is vital when investigating intertidal species’ distribution patterns. The thermal sensitivities of two limpets, Cellana grata and C. toreuma, differed in accordance with their vertical distributions. Cardiac performance was maintained at higher temperatures (~47°C) for the high-zone C. grata than the mid-zone C. toreuma (~42°C). At 40°C, C. grata maintained regular heart function for ~4 h, while heart function of C. toreuma decreased rapidly. Heat shock protein expression revealed that C. toreuma had two constitutive isoforms, Hsp77 and Hsp72, and C. grata one inducible form, Hsp75, which was upregulated at 40°C, suggesting C. grata has a more effective heat shock response than C. toreuma. The temperature-adaptive differences in cardiac thermal tolerance and Hsp expression match observed differences in thermally induced mortalities with the onset of summer and may help predict differential effects of climate change on the two congeners.

Temperature acclimation alters cardiac performance in the lobster Homarus americanus

The American lobster is a poikilotherm that inhabits a marine environment where temperature varies over a 25 degrees C range and depends on the winds, the tides and the seasons. To determine how cardiac performance depends on the water temperature to which the lobsters are acclimated we measured lobster heart rates in vivo. The upper limit for cardiac function in lobsters acclimated to 20 degrees C is approximately 29 degrees C, 5 degrees C warmer than that measured in lobsters acclimated to 4 degrees C. Warm acclimation also slows the lobster heart rate within the temperature range from 4 to 12 degrees C. Both effects are apparent after relatively short periods of warm acclimation (3-14 days). However, warm acclimation impairs cardiac function at cold temperatures: following several hours exposure to frigid (<5 degrees C) temperatures heart rates become slow and arrhythmic in warm acclimated, but not cold acclimated, lobsters. Thus, acclimation temperature determines the thermal limits for cardiac function at both extremes of the 25 degrees C temperature range lobsters inhabit in the wild. These observations suggest that regulation of cardiac thermal tolerance by the prevailing environmental temperature protects against the possibility of cardiac failure due to thermal stress.