Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology
Cardio-respiratory function during exercise in the cobia, Rachycentron canadum: The impact of crude oil exposure
Introduction
All teleost species increase cardiac output and associated oxygen delivery to support increases in swim performance (Farrell, 1991). Increased convective transport by the cardiovascular system is essential to ensure oxygen transport from the respiratory media to the aerobically active tissues (Hillman et al., 2013, Hedrick et al., 2015, Hillman and Hedrick, 2015). As cardiac output is the product of stroke volume and heart rate, adjustments in either or both parameters can modulate convective transport to meet the increasing oxygen demands that accompany aerobic exercise. However, the role of heart rate or stroke volume in driving adjustments in cardiac output may differ between fish species.
Previous studies of several fish species suggest there are differences in the primary parameter used to modulate cardiac output. In brown trout (Salmo trutta), cardiac output increases with swimming speed due to increases in both heart rate and stroke volume with a notable approximate doubling of heart rate (Altimiras et al., 2002). In the largemouth bass (Micropterus salmoides) increases in cardiac output during exercise are attributed to increases in heart rate while stroke volume remains constant. (Cooke et al., 2007). Sockeye salmon (Oncorhynchus nerka) exhibit marked increases in stroke volume as swim speed increases over a wide range of temperatures (Eliason et al., 2013). Atlantic salmon (Salmo salar) exhibit strong correlations between swim speed and heart rate, suggesting heart rate is the primary parameter used to adjust cardiac output in this species (Lucas, 1994). Hence, the dependence on changing heart rate and/or stroke volume to adjust cardiac output to meet increased convective oxygen transport demands appears to be dictated by species, as well as the conditions, exercise or temperature, that increased metabolic rate. In addition to these naturally occurring environmental factors, anthropogenic challenges, such as crude oil exposure, could also impact cardiovascular function in vivo.
The impact of crude oil exposure, and associated polycyclic aromatic hydrocarbons (PAHs), on organismal physiology has been investigated at multiple levels of biological organization in marine ecosystems (Eisler, 1987, McDowell Capuzzo et al., 1988, Edmunds et al., 2015, Esbaugh et al., 2016, Incardona et al., 2014, Stieglitz et al., 2016, Xu et al., 2016, Mager et al., 2014). Specifically, the detrimental impacts on fish cardiovascular systems have been reported from studies ranging from gene expression to overall organismal function (Edmunds et al., 2015, Incardona et al., 2014, Esbaugh et al., 2016, Stieglitz et al., 2016, Xu et al., 2016, Brette et al., 2014). At the level of the whole organism, our prior studies of the mahi-mahi (Coryphaena hippurus; “mahi” in the following) have documented that PAH exposure compromises swim performance and maximal metabolic rate (Mager et al., 2014, Stieglitz et al., 2016). In our recent study of anesthetized mahi we found that crude oil exposure decreased stroke volume and cardiac contractility (Nelson et al., 2016). These studies provided data suggesting that the deleterious effects of crude oil on swim performance and metabolic rate may be due to compromised cardiac function. However, in vivo investigations of swimming fish are needed to determine if impairments in cardiac function account for the overall reduction in maximal metabolic rate, aerobic scope and swim performance previously documented (Mager et al., 2014, Stieglitz et al., 2016).
Given the variability in the literature regarding the parameters fish use to increase cardiac output and the clear consequences of crude oil exposure on fish aerobic performance, this study was undertaken to first; investigate how cobia (Rachycentron canadum) adjusts heart rate and stroke volume with exercise, and, second; study impacts of oil exposure on cardiac performance during stepwise increases in exercise intensity. We hypothesized that exposure to crude oil would decrease critical swim speed accompanied by reduced cardiac performance.
Section snippets
Animals
Juvenile cobia Rachycentron canadum, (control 382.94 ± 33.13 g n = 8, experimental 354.89 ± 26.15 g n = 9) were maintained in 3000 l fiberglass tanks supplied with flow-through seawater (24–26 °C) at the University of Miami Experimental Hatchery (UMEH). Fish were fed daily to satiation with a mixture of chopped squid, mackerel, and sardines. All fish were fasted for 24 h prior to study. All study procedures were approved by the University of Miami Institutional Animal Care and Use Committee (IACUC protocols
Routine cardiorespiratory performance
Oil exposed fish had an 18% higher heart rate (fH) compared to the control fish (92 ± 2 and 80 ± 3 beats·min− 1, respectively) (p = 0.046; Fig. 1A). In contrast, stroke volume (Vs) was 36% lower (0.39 ± 0.05 ml·kg− 1, 0.61 ± 0.07 ml·kg− 1 respectively) in oil-exposed fish relative to controls (p = 0.02; Fig. 1B). The combined effect was that cardiac output (Q) was similar, control 49.5 ± 6.9 ml·min− 1·kg− 1 and oil exposed 36.4 ± 4.5 ml·min− 1·kg− 1, between the two experimental groups (p = 0.12; Fig. 1C). Likewise,
Discussion
Adjustments in convective oxygen transport during exercise can be achieved through changes in cardiovascular function, blood oxygen saturation and increased arterial venous O2 content difference (Farrell, 2007). In fish species, as in other vertebrates, cardiovascular function adjustments are mediated by changes in both heart rate and stroke volume, however differences in the primary modulator of cardiac output have been reported (Farrell, 1991). While the role of heart rate and stroke volume
Conclusions
Cobia have a large scope for adjusting heart rate and MO2 as they increased by 61% and 390%, respectively, from routine swimming to Ucrit. Ucrit was significantly reduced by oil exposure, which was accompanied by a general reduction in cardiac outputs that was significant at intermediate swim speeds. Collectively, the decreased stroke volume in oil exposed fish was offset by increases in heart rate suggesting homeostatic mechanisms were able to rescue function. Our findings emphasize the need
Acknowledgements
We would especially like to acknowledge the many volunteers and staff at the University of Miami Experimental Hatchery (UMEH) for maintaining the animals as well as Open Blue Sea Farms for supporting the cobia research program at UMEH. This research was made possible by a grant from The Gulf of Mexico Research Initiative. Grant No: SA-1520; Name; Relationship of Effects of Cardiac Outcomes in fish for Validation of Ecological Risk (RECOVER) M. Grosell holds a Maytag Chair of Ichthyology. Data
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