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.

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.

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.