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Baker DW, Matey V, Huynh KT, Wilson JM, Morgan JD, Brauner CJ. Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. Am J Physiol Regul Integr Comp Physiol 296: R1868 -R1880, 2009. First published April 1, 2009 doi:10.1152/ajpregu.90767.2008.-Sturgeons are among the most CO 2 tolerant of fishes investigated to date. However, the basis of this exceptional CO 2 tolerance is unknown. Here, white sturgeon, Acipenser transmontanus, were exposed to elevated CO 2 to investigate the mechanisms associated with short-term hypercarbia tolerance. During exposure to 1.5 kPa PCO 2, transient blood pH [extracellular pH (pHe)] depression was compensated within 24 h and associated with net plasma HCO 3 Ϫ accumulation and equimolar Cl Ϫ loss, and changes in gill morphology, such as a decrease in apical surface area of mitochondrial-rich cells. These findings indicate that pHe recovery at this level of hypercarbia is accomplished in a manner similar to most freshwater teleost species studied to date, although branchial mechanisms involved may differ. White sturgeon exposed to more severe hypercarbia (3 and 6 kPa PCO 2) for 48 h exhibited incomplete pH compensation in blood and red blood cells. Despite pHe depression, intracellular pH (pHi) of white muscle, heart, brain, and liver did not decrease during a transient (6 h of 1.5 kPa PCO 2 ) or prolonged (48 h at 3 and 6 kPa PCO 2) blood acidosis. This pHi protection was not due to high intrinsic buffering in tissues. Such tight active cellular regulation of pHi in the absence of pHe compensation represents a unique pattern for non-air-breathing fishes, and we hypothesize that it is the basis for the exceptional CO 2 tolerance of white sturgeon and, likely, other CO 2 tolerant fishes. Further research to elucidate the specific mechanisms responsible for this tremendous pH regulatory capacity in tissues of white sturgeon is warranted. sturgeon; acid-base regulation; intracellular pH; CO 2 tolerance; hypercarbia/hypercapnia AQUATIC HYPERCARBIA (elevated PCO 2 in water) occurs in fresh and estuarine systems, and Pw CO 2 levels as great as 8 kPa (20-to 30-fold increase over the resting arterial Pa CO 2 of fish) have been observed (24,55) (16)] changes at the gill. These changes in branchial morphology and acid-base-relevant ion transporters may aid with the net acid secretion or base absorption mechanisms necessary to promote blood pH compensation (16,20), although direct evidence for this is lacking.Changes in intracellular pH (pHi) in most fish species studied to date are qualitatively similar to, albeit smaller than, blood pH changes during a respiratory acidosis (6, 49). Because function of many cellular components, such as enzyme activity, is pH sensitive, a general acidosis may have severe consequences on cellular processes, including metabolic energy production (25, 50). Only a handful of studies have measured pHi and pHe simultaneously during hypercarbia in fish; these studies...

For many aquatic species, the upper thermal limit (T max ) and the heart failure temperature (T HF ) are only a few degrees away from the species' current environmental temperatures. While the mechanisms mediating temperature-induced heart failure (HF) remain unresolved, energy flow and/or oxygen supply disruptions to cardiac mitochondria may be impacted by heat stress. Recent work using a New Zealand wrasse (Notolabrus celidotus) found that ATP synthesis capacity of cardiac mitochondria collapses prior to T HF . However, whether this effect is limited to one species from one thermal habitat remains unknown. The present study confirmed that cardiac mitochondrial dysfunction contributes to heat stress-induced HF in two additional wrasses that occupy cold temperate (Notolabrus fucicola) and tropical (Thalassoma lunare) habitats. With exposure to heat stress, T. lunare had the least scope to maintain heart function with increasing temperature. Heat-exposed fish of all species showed elevated plasma succinate, and the heart mitochondria from the cold temperate N. fucicola showed decreased phosphorylation efficiencies (depressed respiratory control ratio, RCR), cytochrome c oxidase (CCO) flux and electron transport system (ETS) flux. In situ assays conducted across a range of temperatures using naive tissues showed depressed complex II (CII) and CCO capacity, limited ETS reserve capacities and lowered efficiencies of pyruvate uptake in T. lunare and N. celidotus. Notably, alterations of mitochondrial function were detectable at saturating oxygen levels, indicating that cardiac mitochondrial insufficiency can occur prior to HF without oxygen limitation. Our data support the view that species distribution may be related to the thermal limits of mitochondrial stability and function, which will be important as oceans continue to warm.

We measured hematocrit and plasma osmolality, cortisol, lactate, glucose, and chloride in wild lake sturgeon Acipenser fulvescens after gill-net capture (24-h sets) and multiple bouts of brief (2-3-min) air exposure during removal from nets and again during measurement and tagging procedures. Our objective was to evaluate the physiological consequences associated with capture, handling, and tagging activities commonly employed during mark-recapture studies and to determine whether blood chemistry values moved toward a resting state after a 3-d recovery period. Lake sturgeon that were caught during spring tagging activities showed plasma cortisol, glucose, lactate, osmolality, and chloride levels similar to those exhibited by maximally stressed lake sturgeon in published laboratory studies. After the 3-d recovery period, all physiological stress indicators had approached a nonstressed state and the values were similar to those previously reported for resting lake sturgeon. It appears that capture-mark-recapture programs that subject lake sturgeon to stressors similar to those applied here do not pose a significant threat to this often legislatively protected species.

SUMMARY

SUMMARYIt was hypothesised that chronic hypoxia acclimation (preconditioning) would alter the behavioural low-O 2 avoidance strategy of fish as a result of both aerobic and anaerobic physiological adaptations. Avoidance and physiological responses of juvenile snapper (Pagrus auratus) were therefore investigated following a 6week period of moderate hypoxia exposure (10.2-12.1kPa P O2 , 21±1°C) and compared with those of normoxic controls (P O2 =20-21kPa, 21±1°C). The critical oxygen pressure (P crit ) limit of both groups was unchanged at ~7kPa, as were standard, routine and maximum metabolic rates. However, hypoxia-acclimated fish showed increased tolerances to hypoxia in behavioural choice chambers by avoiding lower P O2 levels (3.3±0.7 vs 5.3±1.1kPa) without displaying greater perturbations of lactate or glucose. This behavioural change was associated with unexpected physiological adjustments. For example, a decrease in blood O 2 carrying capacity was observed after hypoxia acclimation. Also unexpected was an increase in whole-blood P 50 following acclimation to low O 2 , perhaps facilitating Hb-O 2 off-loading to tissues. In addition, cardiac mitochondria measured in situ using permeabilised fibres showed improved O 2 uptake efficiencies. The proportion of the anaerobic enzyme lactate dehydrogenase, at least relative to the aerobic marker enzyme citrate synthase, also increased in heart and skeletal red muscle, indicating enhanced anaerobic potential, or in situ lactate metabolism, in these tissues. Overall, these data suggest that a prioritization of O 2 delivery and O 2 utilisation over O 2 uptake during long-term hypoxia may convey a significant survival benefit to snapper in terms of behavioural low-O 2 tolerance.

The regulation of vertebrate acid-base balance during acute episodes of elevated internal P CO2 is typically characterized by extracellular pH ( pH e ) regulation. Changes in pH e are associated with qualitatively similar changes in intracellular tissue pH ( pH i ) as the two are typically coupled, referred to as 'coupled pH regulation'. However, not all vertebrates rely on coupled pH regulation; instead, some preferentially regulate pH i against severe and maintained reductions in pH e . Preferential pH i regulation has been identified in several adult fish species and an aquatic amphibian, but never in adult amniotes. Recently, common snapping turtles were observed to preferentially regulate pH i during development; the pattern of acid-base regulation in these species shifts from preferential pH i regulation in embryos to coupled pH regulation in adults. In this Commentary, we discuss the hypothesis that preferential pH i regulation may be a general strategy employed by vertebrate embryos in order to maintain acid-base homeostasis during severe acute acid-base disturbances. In adult vertebrates, the retention or loss of preferential pH i regulation may depend on selection pressures associated with the environment inhabited and/or the severity of acid-base regulatory challenges to which they are exposed. We also consider the idea that the retention of preferential pH i regulation into adulthood may have been a key event in vertebrate evolution, with implications for the invasion of freshwater habitats, the evolution of air breathing and the transition of vertebrates from water to land.

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