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

Abstract

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 (massspecific rate of oxygen consumption, Ṁ O2 ) to thermal ramping (21-29°C) and the upper thermal tolerance limit (U TL ) of two intertidal triplefin fishes (Bellapiscis medius and Forsterygion lapillum) under hyperoxia and normoxia. Hyperoxia increased maximal oxygen consumption (Ṁ O2,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.

Acute high temperature exposure impairs hypoxia tolerance in an intertidal fish

“…critically high temperatures can occur with intense solar radiation during daytime low tides, but then during the next low tide (~8-11 h later) severe hypoxia can develop under cooler night-time conditions [7][8][9]. However when examining the response of B. medius, a rock pool specialist within the family of New Zealand triplefin fishes, to sequential high temperature then hypoxia exposure we found no evidence of heat shock induced cross-tolerance.…”

“…There were no differences in body mass of fish in each experimental group (ANOVA, DF = 2, F = 1.65, P = 0.21), and the heat shock exposures were implemented following the same protocol as experiment 1. After heat shock, fish were transferred to respirometry chambers to assess S crit using automated intermittent-flow respirometry (see McArley et al, (2018) [8] for detailed respirometry methods). Briefly, respirometers consisted of a cylindrical acrylic chamber fitted with an adjustable stopper, which allowed the chamber volume (60-110 ml) to be adjusted to match fish size.…”

“…Thus, for rock pool organisms such as intertidal fish, cross-tolerance could offer protection against different environmental stressors across consecutive tidal cycles. For example, temperature and oxygen availability in rock pools fluctuate widely, but when low tides roughly align with the middle of the day and night, peak daytime high temperatures occur out of phase with nocturnal hypoxia [1,[5][6][7][8][9]. This is because the conditions associated with high temperature in isolated rock pools in the middle of the day (i.e.…”

“…On the other hand, severe hypoxia can develop in isolated pools at night (i.e. only 8-11 h later) when respiring organisms draw down O 2 at a time of comparatively stable temperatures [8]. Previous studies have demonstrated that high temperature exposure can induce cross-tolerance to hypoxia in fish.…”

“…Todgham et al (2005) [12] observed a peak in cross-tolerance 12-24 h following exposure to heat shock in O. maculosus; thus, as cross-tolerance was only assessed at one time point in the current study, we chose a recovery time (19 h) within the timeframe of peak cross-tolerance in their study. The +8˚C heat shock (21-29˚C) was used because peak temperatures of this magnitude have been observed in rock pools inhabited by B. medius on hot summer days [8]. The more extreme +10˚C (21-31˚C) heat shock was used to gauge how fish would cope with a future climate change scenario, where peak daytime temperatures may become higher in rock pools.…”