Mechanisms of enhanced cardiorespiratory performance under hyperoxia differ with exposure duration in yellowtail kingfish
Data files
May 03, 2024 version files 32.93 KB
-
Data_file_hyperoxia_kingfish.xlsx
-
README.md
Abstract
Hyperoxia has been shown to expand the aerobic capacity of some fishes, although there have been very few studies examining the underlying mechanisms and how they vary across different exposure durations. Here, we investigated cardiorespiratory function of yellowtail kingfish (Seriola lalandi) acutely (~20 hours) and chronically (3-5 weeks) acclimated to hyperoxia (~200 % air saturation). Our results show that aerobic performance of kingfish is limited in normoxia and increases with environmental hyperoxia. Aerobic scope was elevated in both hyperoxia treatments driven by a ~33% increase in maximum O2 uptake (MO2max), although the mechanisms differed across treatments. Fish acutely transferred to hyperoxia primarily elevated tissue O2 extraction, while increased stroke volume-mediated maximum cardiac output was the main driving factor in chronically acclimated fish. Still an improved O2 delivery to the heart in chronic hyperoxia was not the only explanatory factor as such. Here, maximum cardiac output only increased in chronic hyperoxia compared to normoxia when plastic ventricular growth occurred, as increased stroke volume was partly enabled by an ~8-12% larger relative ventricular mass. Our findings suggest that hyperoxia may be used long-term to boost cardiorespiratory function potentially rendering fish more resilient to metabolically challenging events and stages in their life-cycle.
README: Mechanisms of enhanced cardiorespiratory performance under hyperoxia differ with exposure duration in yellowtail kingfish
https://doi.org/10.5061/dryad.n2z34tn3v
Description of the data and file structure
The sheet named "rest, max and scope cardiorespiratory" contains information on the resting, maximum, and scope cardiorespiratory parameters, i.e., MO2 (SMR, maximum MO2 and aerobic scope, mg O2 h-1), cardiac output (ml min-1), stroke volume (ml), heart rate (beats min-1) and arterial venous O2 content difference (A-VO2, mg O2 ml-1). MO2 stands for O2 uptake and SMR for standard metabolic rate. It also includes, fish ID, weight (g), length (cm), EPOC (excess post-exercise O2 consumption, mg O2), EPOC duration (EPOC duration, h) and EPOC repayment rate (mg O2 h-1), ventricular mass (g), relative ventricular mass (%), relative spleen mass (%), haematocrit (%), haemoglobin concentration (g l-1), MCHC (mean corpuscular haemoglobin concentration, g l-1), pH and % compact myocardium (%). The treatments are normoxia, hyperoxia acute, and hyperoxia chronic. Null values for fish 21 is due to severe injury of the fish during the chase protocol, following which the fish was immediately euthanized and sampled. Thus, only resting values are included for this fish. Null values for EPOC, time to EPOC and EPOC repayment are due to the fish not achieving EPOC repayment during the experimental protocol.
The sheet named "continuous cardiorespiratory" contains the continuous cardiorespiratory measurements prior to and immediately following the exhaustive protocol to elicit maximum cardiorespiratory responses. Again, treatments are normoxia, hyperoxia acute and hyperoxia chronic. Cardiorespiratory dynamics were assessed immediately prior to and at six timepoints following the exhaustive protocol and thus comprised: pre-exhaustion values (time 1), immediately after the exhaustive protocol (time 2), and 0.5 (time 3), 1 (Time 4), 2 (Time 5), 3 (Time 6) and 5 h (Time 8) following the exhaustive protocol. Units are MO2 (mg O2 h-1), cardiac output (ml min-1), stroke volume (ml), heart rate (beats min-1) and arterial venous O2 content difference (A-VO2, mg O2 ml-1).
The sheet named "peak responses" contains information on peak and time to peak MO2, cardiac output, stroke volume, heart rate and arterial venous O2 content difference (A-VO2). Again, null values for fish 21 are due the fish being removed before the end of the stress protocol. Units are MO2 (mg O2 h-1), cardiac output (ml min-1), stroke volume (ml), heart rate (beats min-1), and arterial venous O2 content difference (A-VO2, mg O2 ml-1). The unit for time to peak responses is hours (h).
Sharing/Access information
n/a
Code/Software
n/a
Methods
We recorded the rate of whole-animal O2 uptake (MO2) using intermittent-flow respirometry where the % air saturation inside the respirometer was continuously measured using an O2 optode connected to a Firesting O2 system. Automated flush pumps, were set to flush the respirometers for 5 min every 7 min (i.e., 2 min measurement cycles). MO2 was calculated from the slope of the decline in % air saturation between flushes using the following formula: MO2 = (Vr – Vf) × (Δ%Sat/t) × α; where Vr is the volume of the respirometer, Vf is the volume of the fish assuming that 1 g of tissue equals 1 ml of water, Δ%Sat/t is the change in % O2 saturation per time and α is the temperature-, salinity- and atmospheric pressure-dependent solubility coefficient of O2. The first ~30 s of each measurement cycle was excluded from the slope determination to ensure the inclusion of only the linear section of the decline in O2. SMR (standard metabolic rate) was calculated as the mean of the lowest 20% of all MO2 values obtained throughout the whole 20+ hours of recordings, with measurements 2 standard deviations below the mean of the lowest 20% removed as outliers. MO2max (maximum O2 uptake) was calculated as the highest MO2 value obtained at any point following exercise. The lowest 20% were chosen instead of the more commonly used lowest 10% to maximize the number of fish that achieve EPOC repayment for each treatment. Aerobic scope was then calculated as the difference between SMR and MO2max. EPOC (excess post-exercise O2 consumption) was calculated as the area between the MO2 curve following the stress protocol and SMR + 10% using GraphPad Prism 9.1.2. Briefly, before analysis, individual MO2 traces were smoothed by removing routine MO2 values that were 10% larger than the previous value. EPOC duration was defined as the time in hours between the exhaustive protocol and the intersection of the MO2 trace with the individual SMR + 10%. The rate of EPOC repayment was defined as EPOC/EPOC duration. We cleaned the respirometers thoroughly after each trial, and measured background respiration before and after each individual experiment and was negligible throughout the study (< 0.2% of the MO2 slope).
Heart rate was calculated from the pulsating blood flow signal, and stroke volume was calculated as cardiac output/heart rate. The arterial-venous O2 difference was estimated as MO2/cardiac output (Fick´s principle´s equation). All cardiovascular variables were measured simultaneously with MO2 recordings, and cardiovascular variables measured concomitantly to SMR, MO2max and aerobic scope are referred to henceforth as resting, maximum and scope. Additionally, cardiorespiratory dynamics were assessed immediately prior to and at six time points following the exhaustive protocol and thus comprised: pre-exhaustion values (average of two last cycles prior to exhaustive protocol), immediately after the exhaustive protocol (0 h), and 0.5, 1, 2, 3 and 5 h following the exhaustive protocol. All measurements were derived from the average of two MO2 cycles, except for the 0 h value, which was taken during the first measurement immediately after the exhaustive protocol. Additionally, peak cardiorespiratory responses (i.e., the highest arterial-venous O2 content difference, cardiac output, stroke volume and heart rate measured at any time point throughout the recovery period independently from MO2max) and time to peak cardiorespiratory responses (i.e., the time elapsed from the beginning of the cardiorespiratory measurements following exhaustive exercise to the peak responses) were determined for each fish.
The relative ventricular mass was calculated as wet mass of the ventricle/body mass × 100. To determine the relative % of ventricular compact myocardium, the spongy and compact layers were separated, dried and weighed. The percentage compact myocardium was calculated as dry mass of compact myocardium/dry mass of ventricle × 100. The relative spleen mass was calculated as wet mass of the spleen/body mass × 100.