Mechanisms of enhanced cardiorespiratory performance under hyperoxia differ with exposure duration in yellowtail kingfish.

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 the cardiorespiratory function of yellowtail kingfish (Seriola lalandi) acutely (~20 h) and chronically (3-5 weeks) acclimated to hyperoxia (~200% air saturation). Our results show that the aerobic performance of kingfish is limited in normoxia and increases with environmental hyperoxia. The 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 with 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.

Beating the heart failure odds: long-term survival after myocardial ischemia in juvenile rainbow trout.

Salmonid fish include some of the most valued cultured fish species worldwide. Unlike most other fish, the hearts of salmonids, including Atlantic salmon and rainbow trout, have a well-developed coronary circulation. Consequently, their hearts' reliance on oxygenation through coronary arteries leaves them prone to coronary lesions, believed to precipitate myocardial ischemia. Here, we mimicked such coronary lesions by subjecting groups of juvenile rainbow trout to coronary ligation, assessing histomorphological myocardial changes associated with ischemia and scarring in the context of cardiac arrhythmias using electrocardiography (ECG). Notable ECG changes resembling myocardial ischemia-like ECG in humans, such as atrioventricular blocks and abnormal ventricular depolarization (prolonged and fragmented QRS complex), as well as repolarization (long QT interval) patterns, were observed during the acute phase of myocardial ischemia. A remarkable 100% survival rate was observed among juvenile trout subjected to coronary ligation after 24 wk. Recovery from coronary ligation occurred through adaptive ventricular remodeling, coupled with a fast cardiac revascularization response. These findings carry significant implications for understanding the mechanisms governing cardiac health in salmonid fish, a family particularly susceptible to cardiac diseases. Furthermore, our results provide valuable insights into comparative studies on the evolution, pathophysiology, and ontogeny of vertebrate cardiac repair and restoration.NEW & NOTEWORTHY Juvenile rainbow trout exhibit a remarkable capacity to recover from cardiac injury caused by myocardial ischemia. Recovery from cardiac damage occurs through adaptive ventricular remodeling, coupled with a rapid cardiac revascularization response. These findings carry significant implications for understanding the mechanisms governing cardiac health within salmonid fishes, which are particularly susceptible to cardiac diseases.

Metabolic resilience of the Australasian snapper (Chrysophrys auratus) to marine heatwaves and hypoxia.

Marine organisms are under threat from a simultaneous combination of climate change stressors, including warming sea surface temperatures (SST), marine heatwave (MHW) episodes, and hypoxic events. This study sought to investigate the impacts of these stressors on the Australasian snapper (C. auratus) - a finfish species of high commercial and recreational importance, from the largest snapper fishery in Aotearoa New Zealand (SNA1). A MHW scenario was simulated from 21°C (current February SST average for north-eastern New Zealand) to a future predicted level of 25°C, with the whole-animal and mitochondrial metabolic performance of snapper in response to hypoxia and elevated temperature tested after 1-, 10-, and 30-days of thermal challenge. It was hypothesised that key indicators of snapper metabolic performance would decline after 1-day of MHW stress, but that partial recovery might arise as result of thermal plasticity after chronic (e.g., 30-day) exposures. In contrast to this hypothesis, snapper performance remained high throughout the MHW: 1) Aerobic metabolic scope increased after 1-day of 25°C exposure and remained high. 2) Hypoxia tolerance, measured as the critical O2 pressure and O2 pressure where loss of equilibrium occurred, declined after 1-day of warm-acclimation, but recovered quickly with no observable difference from the 21°C control following 30-days at 25°C. 3) The performance of snapper mitochondria was also maintained, with oxidative phosphorylation respiration and proton leak flux across the inner mitochondrial membrane of the heart remaining mostly unaffected. Collectively, the results suggest that heart mitochondria displayed resilience, or plasticity, in snapper chronically exposed to 25°C. Therefore, contrary to the notion of climate change having adverse metabolic effects, future temperatures approaching 25°C may be tolerated by C. auratus in Northern New Zealand. Even in conjunction with supplementary hypoxia, 25°C appears to represent a metabolically optimal temperature for this species.

Increased reliance on coronary perfusion for cardiorespiratory performance in seawater-acclimated rainbow trout.

Salmonid ventricles are composed of spongy and compact myocardium, the latter being perfused via a coronary circulation. Rainbow trout (Oncorhynchus mykiss) acclimated to sea water have higher proportions of compact myocardium and display stroke volume-mediated elevations in resting cardiac output relative to freshwater-acclimated trout, probably to meet the higher metabolic needs of osmoregulatory functions. Here, we tested the hypothesis that cardiorespiratory performance of rainbow trout in sea water is more dependent on coronary perfusion by assessing the effects of coronary ligation on cardiorespiratory function in resting and exhaustively exercised trout acclimated to fresh water or sea water. While ligation only had minor effects on resting cardiorespiratory function across salinities, cardiac function after chasing to exhaustion was impaired, presumably as a consequence of atrioventricular block. Ligation reduced maximum O2 consumption rate by 33% and 17% in fish acclimated to sea water and fresh water, respectively, which caused corresponding 41% and 17% reductions in aerobic scope. This was partly explained by different effects on cardiac performance, as maximum stroke volume was only significantly impaired by ligation in sea water, resulting in 38% lower maximum cardiac output in seawater compared with 28% in fresh water. The more pronounced effect on respiratory performance in sea water was presumably also explained by lower blood O2 carrying capacity, with ligated seawater-acclimated trout having 16% and 17% lower haemoglobin concentration and haematocrit, respectively, relative to ligated freshwater trout. In conclusion, we show that the coronary circulation allows seawater-acclimated trout to maintain aerobic scope at a level comparable to that in fresh water.

Continuous gastric saline perfusion elicits cardiovascular responses in freshwater rainbow trout (Oncorhynchus mykiss).

When in seawater, rainbow trout (Oncorhynchus mykiss) drink to avoid dehydration and display stroke volume (SV) mediated elevations in cardiac output (CO) and an increased proportion of CO is diverted to the gastrointestinal tract as compared to when in freshwater. These cardiovascular alterations are associated with distinct reductions in systemic and gastrointestinal vascular resistance (RSys and RGI, respectively). Although increased gastrointestinal blood flow (GBF) is likely essential for osmoregulation in seawater, the sensory functions and mechanisms driving the vascular resistance changes and other associated cardiovascular changes in euryhaline fishes remain poorly understood. Here, we examined whether internal gastrointestinal mechanisms responsive to osmotic changes mediate the cardiovascular changes typically observed in seawater, by comparing the cardiovascular responses of freshwater-acclimated rainbow trout receiving continuous (for 4 days) gastric perfusion with half-strength seawater (½ SW, ~ 17 ppt) to control fish (i.e., no perfusion). We show that perfusion with ½ SW causes significantly larger increases in CO, SV and GBF, as well as reductions in RSys and RGI, compared with the control, whilst there were no significant differences in blood composition between treatments. Taken together, our data suggest that increased gastrointestinal luminal osmolality is sensed directly in the gut, and at least partly, mediates cardiovascular responses previously observed in SW acclimated rainbow trout. Even though a potential role of mechano-receptor stimulation from gastrointestinal volume loading in eliciting these cardiovascular responses cannot be excluded, our study indicates the presence of internal gastrointestinal milieu-sensing mechanisms that affect cardiovascular responses when environmental salinity changes.

Normoxic limitation of maximal oxygen consumption rate, aerobic scope and cardiac performance in exhaustively exercised rainbow trout (Oncorhynchus mykiss).

In fish, maximum O2 consumption rate (MO2,max) and aerobic scope can be expanded following exhaustive exercise in hyperoxia; however, the mechanisms explaining this are yet to be identified. Here, in exhaustively exercised rainbow trout (Oncorhynchus mykiss), we assessed the influence of hyperoxia on MO2,max, aerobic scope, cardiac function and blood parameters to address this knowledge gap. Relative to normoxia, MO2,max was 33% higher under hyperoxia, and this drove a similar increase in aerobic scope. Cardiac output was significantly elevated under hyperoxia at MO2,max because of increased stroke volume, indicating that hyperoxia released a constraint on cardiac contractility apparent with normoxia. Thus, hyperoxia improved maximal cardiac performance, thereby enhancing tissue O2 delivery and allowing a higher MO2,max. Venous blood O2 partial pressure (PvO2) was elevated in hyperoxia at MO2,max, suggesting a contribution of improved luminal O2 supply in enhanced cardiac contractility. Additionally, despite reduced haemoglobin and higher PvO2, hyperoxia treated fish retained a higher arterio-venous O2 content difference at MO2,max. This may have been possible because of hyperoxia offsetting declines in arterial oxygenation that are known to occur following exhaustive exercise in normoxia. If this occurs, increased contractility at MO2,max with hyperoxia may also relate to an improved O2 supply to the compact myocardium via the coronary artery. Our findings show MO2,max and aerobic scope may be limited in normoxia following exhaustive exercise as a result of constrained maximal cardiac performance and highlight the need to further examine whether or not exhaustive exercise protocols are suitable for eliciting MO2,max and estimating aerobic scope in rainbow trout.

Coronary blood flow influences tolerance to environmental extremes in fish.

Approximately half of all fishes have, in addition to the luminal venous O2 supply, a coronary circulation supplying the heart with fully oxygenated blood. Yet, it is not fully understood how coronary O2 delivery affects tolerance to environmental extremes such as warming and hypoxia. Hypoxia reduces arterial oxygenation, while warming increases overall tissue O2 demand. Thus, as both stressors are associated with reduced venous O2 supply to the heart, we hypothesised that coronary flow benefits hypoxia and warming tolerance. To test this hypothesis, we blocked coronary blood flow (via surgical coronary ligation) in rainbow trout (Oncorhynchus mykiss) and assessed how in vivo cardiorespiratory performance and whole-animal tolerance to acute hypoxia and warming was affected. While coronary ligation reduced routine stroke volume relative to trout with intact coronaries, cardiac output was maintained by an increase in heart rate. However, in hypoxia, coronary-ligated trout were unable to increase stroke volume to maintain cardiac output when bradycardia developed, which was associated with a slightly reduced hypoxia tolerance. Moreover, during acute warming, coronary ligation caused cardiac function to collapse at lower temperatures and reduced overall heat tolerance relative to trout with intact coronary arteries. We also found a positive relationship between individual hypoxia and heat tolerance across treatment groups, and tolerance to both environmental stressors was positively correlated with cardiac performance. Collectively, our findings show that coronary perfusion improves cardiac O2 supply and therefore cardiovascular function at environmental extremes, which benefits tolerance to natural and anthropogenically induced environmental perturbations.

Cardiorespiratory adjustments to chronic environmental warming improve hypoxia tolerance in European perch (Perca fluviatilis).

Aquatic hypoxia will become increasingly prevalent in the future as a result of eutrophication combined with climate warming. While short-term warming typically constrains fish hypoxia tolerance, many fishes cope with warming by adjusting physiological traits through thermal acclimation. Yet, little is known about how such adjustments affect tolerance to hypoxia. We examined European perch (Perca fluviatilis) from the Biotest enclosure (23°C, Biotest population), a unique ∼1 km2 ecosystem artificially warmed by cooling water from a nuclear power plant, and an adjacent reference site (16-18°C, reference population). Specifically, we evaluated how acute and chronic warming affect routine oxygen consumption rate (MO2,routine) and cardiovascular performance in acute hypoxia, alongside assessment of the thermal acclimation of the aerobic contribution to hypoxia tolerance (critical O2 tension for MO2,routine: Pcrit) and absolute hypoxia tolerance (O2 tension at loss of equilibrium; PLOE). Chronic adjustments (possibly across lifetime or generations) alleviated energetic costs of warming in Biotest perch by depressing MO2,routine and cardiac output, and by increasing blood O2 carrying capacity relative to reference perch acutely warmed to 23°C. These adjustments were associated with improved maintenance of cardiovascular function and MO2,routine in hypoxia (i.e. reduced Pcrit). However, while Pcrit was only partially thermally compensated in Biotest perch, they had superior absolute hypoxia tolerance (i.e. lowest PLOE) relative to reference perch irrespective of temperature. We show that European perch can thermally adjust physiological traits to safeguard and even improve hypoxia tolerance during chronic environmental warming. This points to cautious optimism that eurythermal fish species may be resilient to the imposition of impaired hypoxia tolerance with climate warming.

Elevated CO2 affects anxiety but not a range of other behaviours in juvenile yellowtail kingfish.

Elevated seawater CO2 can cause a range of behavioural impairments in marine fishes. However, most studies to date have been conducted on small benthic species and very little is known about how higher oceanic CO2 levels could affect the behaviour of large pelagic species. Here, we tested the effects of elevated CO2, and where possible the interacting effects of high temperature, on a range of ecologically important behaviours (anxiety, routine activity, behavioural lateralization and visual acuity) in juvenile yellowtail kingfish, Seriola lalandi. Kingfish were reared from the egg stage to 25 days post-hatch in a full factorial design of ambient and elevated CO2 (~500 and ~1000 µatm pCO2) and temperature (21 °C and 25 °C). The effects of elevated CO2 were trait-specific with anxiety the only behaviour significantly affected. Juvenile S. lalandi reared at elevated CO2 spent more time in the dark zone during a standard black-white test, which is indicative of increased anxiety. Exposure to high temperature had no significant effect on any of the behaviours tested. Overall, our results suggest that juvenile S. lalandi are largely behaviourally tolerant to future ocean acidification and warming. Given the ecological and economic importance of large pelagic fish species more studies investigating the effect of future climate change are urgently needed.

Acute high temperature exposure impairs hypoxia tolerance in an intertidal fish.

Acute heat shock has previously been shown to improve subsequent low O2 (hypoxia) tolerance in an intertidal fish species, a process known as cross-tolerance, but it is not known whether this is a widespread phenomenon. This study examined whether a rock pool specialist, the triplefin fish Bellapiscis medius, exhibits heat shock induced cross-tolerance to hypoxia, i.e., longer time to loss of equilibrium (LOE) and lower critical O2 saturation (Scrit) after recovering from an acute heat challenge. Non-heat shock controls had a median time to loss of equilibrium (LOE50) of 54.4 min under severe hypoxia (7% of air saturation) and a Scrit of 15.8% air saturation. Contrary to expectations, however, treatments that received an 8 or 10°C heat shock showed a significantly shorter LOE50 in hypoxia (+8°C = 41.5 min; +10°C = 28.7 min) and no significant change in Scrit (+8°C = 17.0% air saturation; +10°C = 18.3% of air saturation). Thus, there was no evidence of heat shock induced cross-tolerance to hypoxia in B. medius because exposure to acute heat shock impaired hypoxia tolerance.

Intertidal triplefin fishes have a lower critical oxygen tension (Pcrit), higher maximal aerobic capacity, and higher tissue glycogen stores than their subtidal counterparts.

Decreased oxygen (O2) availability (hypoxia) is common in rock pools and challenges the aerobic metabolism of fishes living in these habitats. In this study, the critical O2 tension (Pcrit), a whole animal measure of the aerobic contribution to hypoxia tolerance, was compared between four New Zealand triplefin fishes including an intertidal specialist (Bellapiscis medius), an occasional intertidal inhabitant (Forsterygion lapillum) and two exclusively subtidal species (F. varium and F. malcolmi). The intertidal species had lower Pcrit values than the subtidal species indicating traits to meet resting O2 demands at lower O2 tensions. While resting O2 demand (standard metabolic rate; SMR) did not show a major difference between species, the intertidal species had higher maximal rates of O2 consumption ([Formula: see text]) and higher aerobic metabolic scope (MS). The high O2 extractive capacity of the intertidal species was associated with increased blood O2 carrying capacity (i.e., higher Hb concentration), in addition to higher mass-specific gill surface area and thinner gill secondary lamellae that collectively conveyed a higher capacity for O2 flux across the gills. The specialist intertidal species B. medius also had higher glycogen stores in both white muscle and brain tissues, suggesting a greater potential to generate ATP anaerobically and survive in rock pools with O2 tensions less than Pcrit. Overall, this study shows that the superior Pcrit of intertidal triplefin species is not linked to a minimisation of SMR, but is instead associated with an increased O2 extractive capacity of the cardiorespiratory system (i.e., [Formula: see text], MS, Hb and gill O2 flux).

Hyperoxia increases maximum oxygen consumption and aerobic scope of intertidal fish facing acutely high temperatures.

Daytime low tides that lead to high-temperature events in stranded rock pools often co-occur with algae-mediated hyperoxia as a result of strong solar radiation. Recent evidence shows aerobic metabolic scope (MS) can be expanded under hyperoxia in fish but so far this possibility has not been examined in intertidal species despite being an ecologically relevant scenario. Furthermore, it is unknown whether hyperoxia increases the upper thermal tolerance limits of intertidal fish and, therefore, their ability to withstand extreme high-temperature events. Therefore, we measured the metabolic response (mass-specific rate of oxygen consumption, MO2 ) to thermal ramping (21-29°C) and the upper thermal tolerance limit (UTL) of two intertidal triplefin fishes (Bellapiscis medius and Forsterygion lapillum) under hyperoxia and normoxia. Hyperoxia increased maximal oxygen consumption (MO2,max) and MS of each species at ambient temperature (21°C) but also after thermal ramping to elevated temperatures such as those observed in rock pools (29°C). While hyperoxia did not provide a biologically meaningful increase in upper thermal tolerance of either species (>31°C under all conditions), the observed expansion of MS at 29°C under hyperoxia could potentially benefit the aerobic performance, and hence the growth and feeding potential, etc., of intertidal fish at non-critical temperatures. That hyperoxia does not increase upper thermal tolerance in a meaningful way is cause for concern as climate change is expected to drive more extreme rock pool temperatures in the future and this could present a major challenge for these species.

Chronic warm exposure impairs growth performance and reduces thermal safety margins in the common triplefin fish (Forsterygion lapillum).

Intertidal fish species face gradual chronic changes in temperature and greater extremes of acute thermal exposure through climate-induced warming. As sea temperatures rise, it has been proposed that whole-animal performance will be impaired through oxygen and capacity limited thermal tolerance [OCLTT; reduced aerobic metabolic scope (MS)] and, on acute exposure to high temperatures, thermal safety margins may be reduced because of constrained acclimation capacity of upper thermal limits. Using the New Zealand triplefin fish (Forsterygion lapillum), this study addressed how performance in terms of growth and metabolism (MS) and upper thermal tolerance limits would be affected by chronic exposure to elevated temperature. Growth was measured in fish acclimated (12 weeks) to present and predicted future temperatures and metabolic rates were then determined in fish at acclimation temperatures and with acute thermal ramping. In agreement with the OCLTT hypothesis, chronic exposure to elevated temperature significantly reduced growth performance and MS. However, despite the prospect of impaired growth performance under warmer future summertime conditions, an annual growth model revealed that elevated temperatures may only shift the timing of high growth potential and not the overall annual growth rate. While the upper thermal tolerance (i.e. critical thermal maxima) increased with exposure to warmer temperatures and was associated with depressed metabolic rates during acute thermal ramping, upper thermal tolerance did not differ between present and predicted future summertime temperatures. This suggests that warming may progressively decrease thermal safety margins for hardy generalist species and could limit the available habitat range of intertidal populations.