Sinoatrial tissue of crucian carp heart has only negative contractile responses to autonomic agonists

Background  

In the anoxia-tolerant crucian carp (Carassius carassius) cardiac activity varies according to the seasons. To clarify the role of autonomic nervous control in modulation of cardiac activity, responses of atrial contraction and heart rate (HR) to carbacholine (CCh) and isoprenaline (Iso) were determined in fish acclimatized to winter (4°C, cold-acclimated, CA) and summer (18°C, warm-acclimated, WA) temperatures.     

The effect of acute warming and thermal acclimation on maximum heart rate of the common killifish Fundulus heteroclitus

Common killifish Fundulus heteroclitus were acclimated to ecologically relevant temperatures (5, 15 and 33°C) and their maximum heart rate (f_Hmax) was measured at each acclimation temperature during an acute warming protocol. Acclimation to 33°C increased peak f_Hmax by up to 32% and allowed the heart to beat rhythmically at a temperature 10°C higher when compared with acclimation to 5°C. Independent of acclimation temperature, peak f_Hmax occurred about 3°C cooler than the temperature that first produced cardiac arrhythmias. Thus, when compared with previously published values for the critical thermal maximum of F. heteroclitus, the temperature for peak f_Hmax was cooler and the temperature that first produced cardiac arrhythmias was similar to these critical thermal maxima. The considerable thermal plasticity of f_Hmax demonstrated in the present study is entirely consistent with eurythermal ecology of killifish, as shown previously for another eurythermal fish Gillichthys mirabilis.     

Effects of acute temperature changes on gut physiology in two species of sculpin from the west coast of Greenland

For a fish to thrive, the gut must function efficiently. This is achieved through a range of processes, including controlled patterns of gut motility and modifications in gut blood flow. The knowledge of how gut functions in fish are affected by environmental temperature is sparse, and in order to understand how changes in climate may affect fish populations, we need to understand how gut blood flow and gut motility are affected by changes in temperature. By simultaneous recording of gut blood flow, gut motility, cardiac output, heart rate and cardiac stroke volume, in vivo at 4, 9 and 14 °C, the acute thermal sensitivity of a thermal generalist (shorthorn sculpin Myoxocephalu scorpius) was compared to the more strictly Arctic species (Arctic sculpin M. scorpioides). Temperature effects on gut motility were further explored in vitro, using isolated smooth muscles. Elevated water temperatures increased gut blood flow and contractile activity. Contraction frequency increased nearly threefold and gut blood flow almost doubled with the 10 °C increase. Both cardiac output and heart rate increased with temperature, while cardiac stroke volume decreased. The cholinergic agonist carbachol was most potent on smooth muscles at 9 °C. There were no differences between the two species, suggesting that the gastrointestinal and cardiovascular systems of Arctic sculpin, although a more pronounced Arctic species, have similar abilities to cope with acute fluctuations in water temperature as shorthorn sculpin. The impact of increased gut activity at higher temperatures needs further investigation before the effects of climate change can be predicted.     

Responses of the killifish (Aphanius dispar) to long-term exposure to elevated temperatures: growth,survival and microstructure of gill and heart tissues

Some fish species, such as killifish, that normally inhabit temperate water environments are also found in extreme thermal environments such as thermal springs. The extent of the adaptations involved is not known. In the present laboratory study, we exposed killifish (Aphanius dispar) acclimated to a normal thermal environment to elevated temperatures (37–40 °C) in which related killifish species live permanently. Our objective was to determine whether there is evidence that killifish have heat-shock characteristics that make permanent adaptation likely. The fish was exposed to this temperature for a period of 44 days and then compared with control fish kept at their normal temperature (24 °C) with respect to growth, survival and histopathology of gill and heart tissues. At the end of the experimental time, the percentage of body weight gain and specific growth rate were significantly lower in fish kept in thermal stress compared with the control group. Feed conversion ratio (FCR) was also significantly affected by water temperature, so that during thermal stress the values of FCR were negative. Fish condition (Condition factor: CF) did not differ significantly between both groups at the end of the experiment. On days 11 and 33, however, CF was significantly lower in the thermal stress group. The gill showed blood congestion in primary lamellae and shortened secondary lamellae in fish kept at 37–40 °C. No specific alterations were found in the cardiac tissue of fish kept in thermal stress conditions. Under thermal stress, 40% of fish survived until the end of the experiment. A preliminary conclusion drawn from this work is that A. dispar, which lives at normal temperatures, shows evidence of adaptability to elevated temperatures that could be a factor in the ability of killifish to adapt permanently over time to thermal environment.     

Thermal maxima for juvenile shortnose sturgeon acclimated to different temperatures

Many populations of shortnose sturgeon, Acipenser brevirostrum, in the southeastern United States continue to suffer from poor juvenile recruitment. High summer water temperatures, which may be exacerbated by anthropogenic activities, are thought to affect recruitment by limiting available summer habitat. However, information regarding temperature thresholds of shortnose sturgeon is limited. In this study, the thermal maximum method and a heating rate of 0.1°C min⁻¹ was used to determine critical and lethal thermal maxima for young-of-the-year (YOY) shortnose sturgeon acclimated to temperatures of 19.5 and 24.1°C. Fish used in the experiment were 0.6 to 35.0 g in weight and 64 to 140 days post hatch (dph) in age. Critical thermal maxima were 33.7°C (±0.3) and 35.1°C (±0.2) for fish acclimated to 19.5 and 24.1°C, respectively. Critical thermal maxima significantly increased with an increase in acclimation temperature (p < 0.0001). Lethal thermal maxima were 34.8°C (±0.1) and 36.1°C (±0.1) for fish acclimated to 19.5 and 24.1°C, respectively. Lethal thermal maxima were significantly affected by acclimation temperature, the log₁₀ (fish weight), and the interaction between log₁₀(fish weight) and acclimation temperature (p < 0.0001). Thermal maxima were used to estimate upper limits of safe temperature, thermal preferences, and optimal growth temperatures of YOY shortnose sturgeon. Upper limits of safe temperature were similar to previous temperature tolerance information and indicate that summer temperatures in southeastern rivers may be lethal to YOY shortnose sturgeon if suitable thermal refuge cannot be found.     

Cold acclimation increases basal heart rate but decreases its thermal tolerance in rainbow trout (Oncorhynchus mykiss)

Rainbow trout (Oncorhynchus mykiss, Walbaum) were acclimated to 4 degrees C and 17 degrees C for more than 4 weeks and heart rate was determined in the absence and presence of adrenaline to see how thermal adaptation influences basal heart rate and its beta-adrenergic control in a eurythermal fish species. The basal heart rate in vitro was higher in cold-acclimated than warm-acclimated rainbow trout at temperatures below 17 degrees C. On the other hand, adaptation to cold decreased thermal tolerance of heart rate so that the maximal heart rates were achieved at 17 degrees C (75 +/- 4 bpm) and 24 degrees C (88 +/- 2 bpm) in cold-acclimated and warm-acclimated trout, respectively. Beta-adrenergic response of the heart was enhanced by cold-adaptation, since adrenaline (100 nmol l(-1)) caused stronger stimulation of heart rate in cold-acclimated (29 +/- 14%) than in warm-acclimated fish (10 +/- 1%; P = 0.03). Furthermore, adrenaline strongly opposed the temperature-dependent deterioration of force production in cold-acclimated trout but not in warm-acclimated trout. The results indicate that adaptation to cold increases basal heart rate but decreases its thermal tolerance in rainbow trout. Cold acclimation up-regulates the beta-adrenergic system, and beta-adrenoceptor activation seems to provide cardioprotection against high temperatures in the cold-adapted rainbow trout.     

Benefits of thermal acclimation in a tropical aquatic ectotherm,the Arafura filesnake, <Emphasis Type="Italic">Acrochordus arafurae</Emphasis>

The presumption that organisms benefit from thermal acclimation has been widely debated in the literature. The ability to thermally acclimate to offset temperature effects on physiological function is prevalent in ectotherms that are unable to thermoregulate year-round to maintain performance. In this study we examined the physiological and behavioural consequences of long-term exposure to different water temperatures in the aquatic snake Acrochordus arafurae. We hypothesised that long dives would benefit this species by reducing the likelihood of avian predation. To achieve longer dives at high temperatures, we predicted that thermal acclimation of A. arafurae would reduce metabolic rate and increase use of aquatic respiration. Acrochordus arafurae were held at 24 or 32°C for 3 months before dive duration and physiological factors were assessed (at both 24 and 32°C). Although filesnakes demonstrated thermal acclimation of metabolic rate, use of aquatic respiration was thermally independent and did not acclimate. Mean dive duration did not differ between the acclimation groups at either temperature; however, warm-acclimated animals increased maximum and modal dive duration, demonstrating a longer dive duration capacity. Our study established that A. arafurae is capable of thermal acclimation and this confers a benefit to the diving abilities of this snake.     

Some aspects of acclimation to low temperatures in the grain weevils Sitophilus oryzae (L.) and S. granarius (L.)

The ability of Sitophilus oryzae (L.) and S. granarius (L.) to acclimate when transferred from 27°C, a near optimal temperature, to 15° C, a marginal temperature, was examined in terms of chill-coma temperature, dispersal, oxygen consumption and rate of oviposition. The chill-coma temperature of S. oryzae was higher and the increment of acclimation less than that of S. granarius. Acclimation, although well advanced after 2 weeks after transfer, took more than 4 weeks to complete. Re-acclimation after the reciprocal transfer took only 2 weeks. The dispersal of S. oryzae held at 15 and 27° C prior to testing differed when the weevils were released in wheat at 27°C but not when released at 15°C. Cold-acclimated S. granarius dispersed less than warm-acclimated weevils when released in wheat at both 15 and 27°C. The activity oxygen consumption of cold-acclimated weevils was less than that of warm-acclimated weevils. Inverse-shifts of acutely determined R-T relationships appeared more significant than changes in temperature sensitivity. Acclimation to 15° C took 8–10 days and re-acclimation to 27°C about 6–8 days. S. oryzae consumed less oxygen per unit of weight than S. granarius but was more temperature sensitive. Resting oxygen consumption, which was less temperature sensitive than activity consumption, also exhibited inverse acclimation in both species. S. granarius showed evidence of inverse acclimation of oviposition rate after acclimation at 15°C.     

Growth and thermal tolerance of a Tibet fish Schizopygopsis younghusbandi juveniles acclimated to three temperature levels

Schizopygopsis younghusbandi is an endemic fish of Tibet characterized by slow growth. Artificial stock enhancement was applied to rebuild the natural population of S. younghusbandi in recent years. However, the optimal growth temperature and thermal tolerance of S. younghusbandi has not been studied, which restricts the production of S. younghusbandi fingerling for stock enhancement. The purpose of this paper is to determine the growth, critical thermal maximum (CTMax), lethal thermal maximum (LTMax) and acclimation response ratio (ARR) of S. younghusbandi juveniles (body weight 5.7 ± 1.2 g) at three acclimation temperature levels (10, 15, 20°C). The results showed that acclimation temperature significantly affected the growth, CTMax, LTMax and ARR of the experimental fish. Largest final weight (7.5 ± 2.3 g) was recorded in 15°C group. At a heating rate of 1°C/30 min, CTMax ranged from 30.98 to 32.01°C and LTMax ranged from 31.76 to 32.31°C in the three acclimation temperatures. Schizopygopsis younghusbandi had lower ARR value (0.097) than most other fish species. Low ARR value indicates that S. younghusbandi may have narrower thermal tolerance range and weaker acclimation ability to global warming. For successful aquaculture of S. younghusbandi juveniles, temperature should be maintained around 15°C.     

Stressor interactions in freshwater habitats: Effects of cold water exposure and food limitation on early‐life growth and upper thermal tolerance in white sturgeon,Acipenser transmontanus

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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°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°C is approximately 29°C, 5°C warmer than that measured in lobsters acclimated to 4°C. Warm acclimation also slows the lobster heart rate within the temperature range from 4 to 12°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°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°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.     

Upper thermal tolerance of wild‐type,domesticated and growth hormone‐transgenic coho salmon Oncorhynchus kisutch

In coho salmon Oncorhynchus kisutch, no significant differences in critical thermal maximum (c. 26·9° C, C_Tmax) were observed among size‐matched wild‐type, domesticated, growth hormone (GH)‐transgenic fish fed to satiation, and GH‐transgenic fish on a ration‐restricted diet. Instead, GH‐transgenic fish fed to satiation had significantly higher maximum heart rate and Arrhenius breakpoint temperature (mean ± s.e. = 17·3 ± 0·1° C, T_AB). These results provide insight into effects of modified growth rate on temperature tolerance in salmonids, and can be used to assess the potential ecological consequences of GH‐transgenic fishes should they enter natural environments with temperatures near their thermal tolerance limits.     

The glutathione-dependent system of antioxidant defense is not modulated by temperature acclimation in muscle tissues from striped bass,Morone saxatilis

Cold temperature generally induces an enhancement of oxidative capacities, a greater content of intracellular lipids, and a remodeling of lipids in biological membranes. These physiological responses may pose a heightened risk of lipid peroxidation (LPO), while warm temperature could result in greater risk of LPO since rates involving reactive oxygen species and LPO will be elevated. The current study examines responses of the glutathione system of antioxidant defense after temperature acclimation. We measured total glutathione (tGSH), and protein levels of GPx1, GPx4, and GST (cardiac and skeletal muscles), and enzymatic activity (skeletal muscle) of glutathione-dependent antioxidants (GPx, GPx4, and GST) in tissues from striped bass (Morone saxatilis) acclimated for six weeks to 7 °C or 25 °C. tGSH of cardiac muscle from cold-acclimated animals was 1.2-times higher than in warm-bodied counterparts, but unchanged with temperature acclimation in skeletal muscle. A second low molecular weight antioxidant, ascorbate was 1.4- and 1.5-times higher in cardiac and skeletal muscle, respectively in warm- than cold-acclimated animals. Despite 1.2-times higher oxidative capacities (as indicated by citrate synthase activity), in skeletal muscle from cold- versus warm-acclimated fish, levels and activities of antioxidant enzymes were similar between acclimation groups. Lipid peroxidation products (as indicated by TBARS), normalized to tissue wet weight, were more than 2-times higher in skeletal muscle from cold- than warm-acclimated animals, however, when normalized to phospholipid content there was no statistical difference between acclimation groups. Our results demonstrate that the physiological changes, associated with acclimation to low temperature in the eurythermal striped bass, are not accompanied by an enhanced antioxidant defense in the glutathione-dependent system.     

Effect of rearing temperature on growth and thermal tolerance of Schizothorax (Racoma) kozlovi larvae and juveniles

Effect of rearing temperature on growth and thermal tolerance of Schizothorax (Racoma) kozlovi Nikolsky larvae and juveniles was investigated. The fish (start at 12 d post hatch) were reared for nearly 6 months at five constant temperatures of 10, 14, 18, 22 and 26 °C. Then juvenile fish being acclimated at three temperatures of 14, 18 and 22 °C were chosen to determine their critical thermal maximum (CTMax) and lethal thermal maximum (LTMax) by using the dynamic method. Growth rate of S. kozlovi larvae and juveniles was significantly influenced by temperature and fish size, exhibiting an increase with increased rearing temperature, but a decline with increased fish size. A significant ontogenetic variation in the optimal temperatures for maximum growth were estimated to be 24.7 °C and 20.6 °C for larvae and juveniles of S. kozlovi, respectively. The results also demonstrated that acclimation temperature had marked effects on their CTMax and LTMax, which ranged from 32.86 °C to 34.54 °C and from 33.79 °C to 34.80 °C, respectively. It is suggested that rearing temperature must never rise above 32 °C for its successful aquaculture. Significant temperature effects on the growth rate and thermal tolerance both exhibit a plasticity pattern. Determination of critical heat tolerance and optima temperature for maximum growth of S. kozlovi is of ecological significance in the conservation and aquaculture of this species.     

Sub-lethal temperature thresholds indicate acclimation and physiological limits in brook trout Salvelinus fontinalis

The upper thermal tolerance of brook trout Salvelinus fontinalis was estimated using critical thermal maxima (CT_max) experiments on fish acclimated to temperatures that span the species' thermal range (5–25°C). The CT_max increased with acclimation temperature but plateaued in fish acclimated to 20, 23 and 25°C. Plasma lactate was highest, and the hepato-somatic index (I_H) was lowest at 23 and 25°C, which suggests additional metabolic costs at those acclimation temperatures. The results suggest that there is a sub-lethal threshold between 20 and 23°C, beyond which the fish experience reduced physiological performance.     

Upper thermal limits of cardiac function for Arctic cod Boreogadus saida,a key food web fish species in the Arctic Ocean

The objective of this study was to determine the upper thermal limits of Arctic cod Boreogadus saida by measuring the response of maximum heart rate (f_Hmax) to acute warming. One set of fish were tested in a field laboratory in Cambridge Bay (CB), Nunavut (north of the Arctic Circle), and a second set were tested after air transport to and 6 month temperature acclimation at the Vancouver Aquarium (VA) laboratory. In both sets of tests, with B. saida acclimated to 0° C, f_Hmax increased during acute warming up to temperatures considerably higher than the acclimation temperature and the near‐freezing Arctic temperatures in which they are routinely found. Indeed, f_Hmax increased steadily between 0·5 and 5·5° C, with no significant difference between the CB and VA tests (P > 0·05) and with an overall mean ± s.e. Q₁₀ of 2·4 ± 0·5. The first Arrhenius breakpoint temperature (T_AB) for f_Hmax was also statistically indistinguishable for the two sets of tests (mean ± s.e. 3·2 ± 0·3 and 3·6 ± 0·3° C), suggesting that the temperature optimum for B. saida could be reliably measured after live transport to a more southerly laboratory location. Continued warming above 5·5° C revealed a large variability among individuals in the upper thermal limits that triggered cardiac arrhythmia (T_arr), ranging from 10·2 to 15·2° C with mean ± s.e. 12·4 ± 0·4° C (n = 11) for the field study. A difference did exist between the CB and VA breakpoint temperatures when the Q₁₀ value decreased below 2 (the Q₁₀ breakpoint temperature; T_QB) at 8·0 and 5·5° C, respectively. These results suggest that factors, other than thermal tolerance and associated cardiac performance, may influence the realized distribution of B. saida within the Arctic Circle.     

Effects of autonomic blockade on acute thermal tolerance and cardioventilatory performance in rainbow trout,Oncorhynchus mykiss

Predicted future increases in global temperature may impose challenges for ectothermic animals like fish, but the physiological mechanisms determining the critical thermal maximum (CT_max) are not well understood. One hypothesis suggests that impaired cardiac performance, limited by oxygen supply, is an important underlying mechanism. Since vagal bradycardia is suggested to improve cardiac oxygenation and adrenergic stimulation may improve cardiac contractility and protect cardiac function at high temperatures, we predicted that pharmacological blockade of cardiac autonomic control would lower CT_max. Rainbow trout was instrumented with a flow probe and a ventilation catheter for cardioventilatory recordings and exposed to an acute thermal challenge until CT_max following selective pharmacological blockade of muscarinic or β-adrenergic receptors.Contrary to our prediction, CT_max (~26 °C) was unchanged between treatments. While β-adrenergic blockade reduced heart rate it did not impair cardiac stroke volume across temperatures suggesting that compensatory increases in cardiac filling pressure may serve to maintain cardiac output. While warming resulted in significant tachycardia and increased cardiac output, a high cholinergic tone on the heart was observed at temperatures approaching CT_max. This may represent a mechanism to maintain scope for heart rate and possibly to improve myocardial contractility and oxygen supply at high temperatures. This is the first study evaluating the importance of autonomic cardiac control on thermal tolerance in fish. While no effects on CT_max were observed, this study raises important questions about the underlying mechanisms determining thermal tolerance limits in ectothermic animals.     

Evidence for developmental thermal acclimation in the damselfish, Pomacentrus moluccensis

Tropical species are predicted to have limited capacity for acclimation to global warming. This study investigated the potential for developmental thermal acclimation by the tropical damselfish Pomacentrus moluccensis to ocean temperatures predicted to occur over the next 50–100 years. Newly settled juveniles were reared for 4 months in four temperature treatments, consisting of the current-day summer average (28.5 °C) and up to 3 °C above the average (29.5, 30.5 and 31.5 °C). Resting metabolic rate (RMR) of fish reared at 29.5 and 31.5 °C was significantly higher than the control group reared at 28.5 °C. In contrast, RMR of fish reared at 30.5 °C was not significantly different from the control group, indicating these fish had acclimated to their rearing temperature. Furthermore, fish that developed in 30.5 and 31.5 °C exhibited an enhanced ability to deal with acute temperature increases. These findings illustrate that developmental acclimation may help coral reef fish cope with warming ocean temperatures.     

Temperature effects on aerobic scope and cardiac performance of European perch (Perca fluviatilis)

Several recent studies have highlighted how impaired cardiac performance at high temperatures and in hypoxia may compromise the capacity for oxygen transport. Thus, at high temperatures impaired cardiac capacity is proposed to reduce oxygen transport to a degree that lowers aerobic scope and compromises thermal tolerance (the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis). To investigate this hypothesis, we measured aerobic and cardiac performance of a eurythermal freshwater teleost, the European perch (Perca fluviatilis). Rates of oxygen consumption were measured during rest and activity at temperatures between 5 °C and 27 °C, and we evaluated cardiac function by in vivo measurements of heart rate and in vitro studies to determine contractility of myocardial strips. Aerobic scope increased progressively from 5 °C to 21 °C, after which it levelled off. Heart rate showed a similar response. We found little difference between resting and active heart rate at high temperature suggesting that increased cardiac scope during activity is primarily related to changes in stroke volume. To examine the effects of temperature on cardiac capacity, we measured isometric force development in electrically paced myocardial preparations during different combinations of temperature, pacing frequency, oxygenation and adrenergic stimulation. The force-frequency product increased markedly upon adrenergic stimulation at 21 and 27 °C (with higher effects at 21 °C) and the cardiac preparations were highly sensitive to hypoxia. These findings suggest that at (critically) high temperatures, cardiac output may diminish due to a decreased effect of adrenergic stimulation and that this effect may be further exacerbated if the heart becomes hypoxic. Hence cardiac limitations may contribute to the inability to increase aerobic scope at high temperatures in the European perch (Perca fluviatilis).     

Upper thermal tolerance of closely related Danio species

The main finding of this study was that measuring maximum heart rate during incremental warming was an effective tool to estimate upper thermal limits in three small cyprinid Danio species, which differed significantly. Arrhenius breakpoint temperature for maximum heart rate, purportedly an index of optimum temperature, was 21·2 ± 0·4, 20·1 ± 0·4 and 18·9 ± 0·8° C (mean ± s.e .) for zebrafish Danio rerio, pearl danio Danio albolineatus and glowlight danio Danio choprae, respectively. The temperature where cardiac arrhythmias were first induced during warming (T_arr) was 36·6 ± 0·7, 36·9 ± 0·8 and 33·2 ± 0·8° C (mean ± s.e .) and critical thermal maximum (T_Cm) was 39·9 ± 0·1, 38·9 ± 0·1 and 37·2 ± 0·1° C (mean ± s.e .) for D. rerio, D. albolineatus and D. choprae, respectively. The finding that T_arr was consistently 3–4° C lower than T_Cm suggests that collapse of the cardiac life support system may be a critical trigger for upper temperature tolerance. The upper thermal limits established here, which correlate well with a broad natural environmental temperature range for D. rerio and a narrow one for D. choprae, suggest that upper thermal tolerance may be a genetic trait even among closely related species acclimated to common temperatures.