Erik Sandblom

Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations

Summary Measurements of aerobic scope [the difference between minimum and maximum oxygen consumption rate ( and , respectively)] are increasing in prevalence as a tool to address questions relating to fish ecology and the effects of climate change. However, there are underlying issues regarding the array of methods used to measure aerobic scope across studies and species. In an attempt to enhance quality control before the diversity of issues becomes too great to remedy, this paper outlines common techniques and pitfalls associated with measurements of , and aerobic scope across species and under different experimental conditions. Additionally, we provide a brief critique of the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis, a concept that is intricately dependent on aerobic scope measurements and is spreading wildly throughout the literature despite little evidence for its general applicability. It is the intention of this paper to encourage transparency and accuracy in future studies that measure the aerobic metabolism of fishes, and to highlight the fundamental issues with assuming broad relevance of the OCLTT hypothesis.

The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka).

SUMMARY The mechanism underlying the decrease in aerobic scope in fish at warm temperatures is not fully understood and is the focus of this research. Our study examined oxygen uptake and delivery in resting, swimming and recovering sockeye salmon while water temperature was acutely increased from 15°C to 24°C in 2°C h–1 increments. Fish swam at a constant speed during the temperature change. By simultaneously measuring oxygen consumption (ṀO2), cardiac output (Q̇) and the blood oxygen status of arterial and venous blood, we were able to determine where in the oxygen cascade a limitation appeared when fish stopped sustained swimming as temperature increased. High temperature fatigue of swimming sockeye salmon was not a result of a failure of either oxygen delivery to the gills or oxygen diffusion at the gills because oxygen partial pressure (PO2) and oxygen content (CO2) in arterial blood did not decrease with increasing temperature, as would be predicted for such limitations. Instead, arterial oxygen delivery (TaO2) was initially hampered due to a failure to adequately increase Q̇ with increasing temperature. Subsequently, lactate appeared in the blood and venous PO2 remained constant.

Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut

As a consequence of increasing atmospheric CO2, the worlds oceans are becoming warmer and more acidic. Whilst the ecological effects of these changes are poorly understood, it has been suggested that fish performance including growth will be reduced mainly as a result of limitations in oxygen transport capacity. Contrary to the predictions given by the oxygen- and capacity-limited thermal tolerance hypothesis, we show that aerobic scope and cardiac performance of Atlantic halibut (Hippoglossus hippoglossus) increase following 14–16 weeks exposure to elevated temperatures and even more so in combination with CO2-acidified seawater. However, the increase does not translate into improved growth, demonstrating that oxygen uptake is not the limiting factor for growth performance at high temperatures. Instead, long-term exposure to CO2-acidified seawater reduces growth at temperatures that are frequently encountered by this species in nature, indicating that elevated atmospheric CO2 levels may have serious implications on fish populations in the future.

Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha)

This study was undertaken to provide a comprehensive set of data relevant to disclosing the physiological effects and possible oxygen transport limitations in the Chinook salmon (Oncorhynchus tshawytscha) during an acute temperature change. Fish were instrumented with a blood flow probe around the ventral aorta and catheters in the dorsal aorta and sinus venosus. Water temperature was progressively increased from 13 degrees C in steps of 4 degrees C up to 25 degrees C. Cardiac output increased from 29 to 56 ml.min(-1).kg(-1) between 13 and 25 degrees C through an increase in heart rate (58 to 105 beats/min). Systemic vascular resistance was reduced, causing a stable dorsal aortic blood pressure, yet central venous blood pressure increased significantly at 25 degrees C. Oxygen consumption rate increased from 3.4 to 8.7 mg.min(-1).kg(-1) during the temperature increase, although there were signs of anaerobic respiration at 25 degrees C in the form of increased blood lactate and decreased pH. Arterial oxygen partial pressure was maintained during the heat stress, although venous oxygen partial pressure (Pv(O(2))) and venous oxygen content were significantly reduced. Cardiac arrhythmias were prominent in three of the largest fish (>4 kg) at 25 degrees C. Given the switch to anaerobic metabolism and the observation of cardiac arrhythmias at 25 degrees C, we propose that the cascade of venous oxygen depletion results in a threshold value for Pv(O(2)) of around 1 kPa. At this point, the oxygen supply to systemic and cardiac tissues is compromised, such that the oxygen-deprived and acidotic myocardium becomes arrhythmic, and blood perfusion through the gills and to the tissues becomes compromised.

Intestinal transport mechanisms and plasma cortisol levels during normal and out-of-season parr–smolt transformation of Atlantic salmon, Salmo salar

Abstract The intestine is one of the major osmoregulatory organs in fish. During the salmon parr–smolt transformation, the intestine must change its functions from the freshwater (FW) role of preventing water inflow, to the seawater (SW) role of actively absorbing ions and water. This development can be assessed as an increased intestinal fluid transport (Jv) during the parr–smolt transformation. The developmental changes taking place during parr–smolt transformation are governed by a number of endocrine systems, of which cortisol is the main stimulator of Jv. In order to further elucidate the mechanisms behind the elevation of Jv during parr–smolt transformation, juvenile Atlantic salmon were followed during natural (1+age) as well as photoperiod-induced (0+age) smoltification. Plasma cortisol levels, gill and intestinal Na + ,K + -ATPase activity, Jv (only during natural smoltification) and intestinal paracellular permeability were measured. In natural smolting as well as in photoperiod-induced smolting, normal patterns of plasma cortisol levels and gill Na + ,K + -ATPase activity, with clearly defined, transient peaks were obtained. When fish were transferred to SW, a second elevation in plasma cortisol levels and gill Na + ,K + -ATPase activity occurred, whereas Jv remained at similar levels as in FW fish. As to the mechanisms behind the increased Jv during parr–smolt transformation, the intestinal Na + ,K + -ATPase activity increases in the anterior intestine and the paracellular permeability, as judged by transepithelial resistance (TER), appears to decrease in the posterior intestine. These events correspond with the increase in Jv seen during this developmental stage. Furthermore, the increase in the physiological parameters follows the changes in plasma cortisol levels, shifted by a couple of weeks. When the fish were transferred to SW, a further increase in Na + ,K + -ATPase activity was apparent in both anterior and posterior intestine and the paracellular permeability decreases. To summarize, the increased Jv seen during the parr–smolt transformation of Atlantic salmon may be due to an increase in the paracellular water flow of the posterior intestine. When the fish enter SW, the water flow appears to be directed from the paracellular pathway towards a more transcellular route with increased intestinal Na + ,K + -ATPase activity as the main driving force.

Sex-specific differences in cardiac control and hematology of sockeye salmon (Oncorhynchus nerka) approaching their spawning grounds

Some male salmonids (e.g., rainbow trout) display profound cardiovascular adjustments during sexual maturation, including cardiac growth and hypertension, and tachycardia has been observed in free-ranging male salmonids near their spawning grounds. In the present study, we investigated cardiac control, dorsal aortic blood pressure, cardiac morphometrics, and hematological variables in wild, sexually maturing sockeye salmon (Oncorhynchus nerka) with a particular aim to decipher any sex-specific differences. Routine heart rate (f(H)) was significantly higher in females (52 vs. 43 beats/min), which was due to significantly lower cholinergic tone (28 vs. 46%), because there were no differences in adrenergic tone or intrinsic heart rate between sexes. No differences in blood pressure were observed despite males possessing an 11% greater relative ventricular mass. Concomitant with higher routine heart rates, female sockeye had significantly higher levels of cortisol, testosterone, and 17beta-estradiol, whereas the level of 11-ketotestosterone was higher in males. There were no differences in hematocrit or hemoglobin concentration between the sexes. The findings of this study highlight the importance of considering sex as a variable in research fields such as conservation biology and when modeling the consequences of local and global climate change. Indeed, this study helps to provide a mechanistic basis for the significantly higher rates of female mortality observed in previous studies of wild-caught sockeye salmon.

Baroreflex mediated control of heart rate and vascular capacitance in trout

SUMMARY The baroreflex was triggered by altering branchial blood pressure with pre- and post-branchial occlusions for 30 s in rainbow trout Oncorhynchus mykiss. The cardiac limb of the baroreflex was monitored by continuous heart rate (fH) measurements. Responses of venous capacitance vessels were assessed, immediately following either occlusion, by measuring mean circulatory filling pressure (MCFP). Arterial responses were evaluated as the change in dorsal aortic blood pressure (Pda) before and after pre-branchial occlusion. In untreated fish pre-branchial occlusion resulted in tachycardia (62.4±2.4 to 69.1±1.7 beats min–1), decreased venous capacitance reflected as an increase in MCFP (0.17±0.03 to 0.27±0.03 kPa) and increased Pda (4.0±0.2 kPa compared to 3.2±0.1 kPa before occlusion). Post-branchial occlusion somewhat reversed the responses since fH decreased (62.4±2.4 to 53.0±3.1 beats min–1), whereas MCFP remained unaltered. Treatment with the α-adrenergic blocker prazosin (1 mg kg–1) increased resting MCFP to 0.33±0.03 kPa and appeared to abolish both venous and arterial responses to branchial occlusion. Subsequent atropine treatment (1.2 mg kg–1) abolished all chronotropic responses. We present for the first time ample evidence for baroreflex-mediated control of cardiovascular homeostasis, including both the chronotropic and the vascular limb of the baroreflex in an unanaesthetized fish. Furthermore, a novel technique to cannulate and occlude the dorsal aorta, using a Fogarty thru-lumen embolectomy catheter, is explained.

Cardiac preload and venous return in swimming sea bass (Dicentrarchus labrax L.)

SUMMARY Cardiac preload (central venous pressure, Pcv), mean circulatory filling pressure (MCFP), dorsal aortic blood pressure (Pda) and relative cardiac output (Q̇) were measured in sea bass (Dicentrarchus labrax) at rest and while swimming at 1 and 2 BL s-1. MCFP, an index of venous capacitance and the upstream venous pressure driving the return of venous blood to the heart, was measured as the plateau in Pcv during ventral aortic occlusion. Compared with resting values, swimming at 1 and 2 BL s-1 increased Q̇ (by 15±1.5 and 38±6.5%, respectively), Pcv (from 0.11±0.01 kPa to 0.12±0.01 and 0.16±0.02 kPa, respectively), MCFP (from 0.27±0.02 kPa to 0.31±0.02 and 0.40±0.04 kPa, respectively) and the calculated pressure gradient for venous return (ΔPv, from 0.16±0.01 kPa to 0.18±0.02 and 0.24±0.02 kPa, respectively), but not Pda. In spite of an increased preload, the increase in Q̇ was exclusively mediated by an increased heart rate (fh, from 80±4 beats min-1 to 88±4 and 103±3 beats min-1, respectively), and stroke volume (Vs) remained unchanged. Prazosin treatment (1 mg kg-1 Mb) abolished pressure and flow changes during swimming at 1 BL s-1, but not 2 BL s-1, indicating that other control systems besides an α-adrenoceptor control are involved. This study is the first to address the control of venous capacitance in swimming fish. It questions the generality that increased Q̇ during swimming is regulated primarily through Vs and shows that an increased cardiac filling pressure does not necessarily lead to an increased Vs in fish, but may instead compensate for a reduced cardiac filling time.

Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia

The ability of an animal to depress ATP turnover while maintaining metabolic energy balance is important for survival during hypoxia. In the present study, we investigated the responses of cardiac energy metabolism and performance in the hypoxia-tolerant tilapia (Oreochromis hybrid sp.) during exposure to environmental hypoxia. Exposure to graded hypoxia (> or =92% to 2.5% air saturation over 3.6 +/- 0.2 h) followed by exposure to 5% air saturation for 8 h caused a depression of whole animal oxygen consumption rate that was accompanied by parallel decreases in heart rate, cardiac output, and cardiac power output (CPO, analogous to ATP demand of the heart). These cardiac parameters remained depressed by 50-60% compared with normoxic values throughout the 8-h exposure. During a 24-h exposure to 5% air saturation, cardiac ATP concentration was unchanged compared with normoxia and anaerobic glycolysis contributed to ATP supply as evidenced by considerable accumulation of lactate in the heart and plasma. Reductions in the provision of aerobic substrates were apparent from a large and rapid (in <1 h) decrease in plasma nonesterified fatty acids concentration and a modest decrease in activity of pyruvate dehydrogenase. Depression of cardiac ATP demand via bradycardia and an associated decrease in CPO appears to be an integral component of hypoxia-induced metabolic rate depression in tilapia and likely contributes to hypoxic survival.

Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future

Temperature acclimation may offset the increased energy expenditure (standard metabolic rate, SMR) and reduced scope for activity (aerobic scope, AS) predicted to occur with local and global warming in fishes and other ectotherms. Yet, the time course and mechanisms of this process is little understood. Acclimation dynamics of SMR, maximum metabolic rate, AS and the specific dynamic action of feeding (SDA) were determined in shorthorn sculpin (Myoxocephalus scorpius) after transfer from 10°C to 16°C. SMR increased in the first week by 82% reducing AS to 55% of initial values, while peak postprandial metabolism was initially greater. This meant that the estimated AS during peak SDA approached zero, constraining digestion and leaving little room for additional aerobic processes. After eight weeks at 16°C, SMR was restored, while AS and the estimated AS during peak SDA recovered partly. Collectively, this demonstrated a considerable capacity for metabolic thermal compensation, which should be better incorporated into future models on organismal responses to climate change. A mathematical model based on the empirical data suggested that phenotypes with fast acclimation rates may be favoured by natural selection as the accumulated energetic cost of a slow acclimation rate increases in a warmer future with exacerbated thermal variations.