Beyond buoyancy and vision: The potential for the Root effect to deliver oxygen to tissues other than the swim bladder and eye (original) (raw)
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Acta Physiologica, 2011
Aim: The ability of high carbon dioxide tensions or low pH to reduce blood oxygen binding even at high oxygen tensions, first observed by August Krogh and Isabella Leitch in 1919 and now known as the Root effect, was studied in red blood cells and haemoglobin solutions of several fish species. Methods: Red blood cells in physiological saline were acidified at atmospheric oxygen tension by increasing carbon dioxide tensions and the percentage decrease in oxygen content was used to quantify the Root effect. Haemoglobin was incubated in air-equilibrated citrate buffers between pH 5 and 7 and the percentage decrease in oxygen saturation relative to pH 8 determined by spectral deconvolution. Results: The maximal magnitude of the Root effect in citrate-buffered haemoglobin solutions closely matched the value in blood or red blood cells of 11 vertebrates over a Root effect range between 3 and 80%. Contrary to previous reports, there was no evidence for a significant Root effect in red blood cells or haemoglobin solutions of the wels catfish, but a significant Root effect under both conditions in the Siberian sturgeon. Conclusions: Under the conditions employed in this study, the maximal Root effect of citrate-buffered haemoglobin solutions closely resembles the maximal Root effect in red blood cells. This strengthens previous studies on the evolution of the Root effect and its role in oxygen concentration at the retina and swimbladder of a large number of fishes that were based on Root effect measurements in haemoglobin solutions.
Kinetics of the Root effect and of O2 exchange in whole blood of the eel
Respiration physiology, 1992
Oxygen transfer kinetics in blood of the eel (Anguilla rostrata, A. anguilla) were measured spectrophotometrically in thin blood layers covered by Gore-Tex membranes, which allowed fast changes of the gas phase at the blood surface (Heidelberger and Reeves, 1990 J. Appl. Physiol. 68: 1854-1864). The following main results were obtained for A. rostrata (similar values were measured for A. anguilla): (1) step change in PO2 of the gas phase between 0 and 37 kPa at low PCO2 (0.19 kPa, blood pH, 8.1; 20 degrees C) yielded mean half times (t(on)) for O2 uptake of 7.1 msec, and for O2 release (t(off)), of 42.8 msec. Similar values were obtained at high PCO2 (19 kPa; blood pH, 6.9), indicating O2 kinetics to be independent of pH and PCO2; (2) decreasing the high PO2 from 37 to 14 kPa significantly prolonged oxygen uptake kinetics, but release kinetics were unaltered; (3) changing PCO2 from 0.19 to 19 kPa at constant high PO2 (37 kPa) resulted in a reduction of hemoglobin oxygen saturation (...
Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish
Proceedings of The Royal Society B: Biological Sciences, 2019
A successful spawning migration in salmon depends on their athletic ability, and thus on efficient cardiovascular oxygen (O 2) transport. Most teleost fishes have highly pH-sensitive haemoglobins (Hb) that can release large amounts of O 2 when the blood is acidified at the tissues. We hypothesized that plasma-accessible carbonic anhydrase (paCA; the enzyme that catalyses proton production from CO 2) is required to acidify the blood at the tissues and promote tissue O 2 extraction. Previous studies have reported an elevated tissue O 2 extraction in hypoxia-acclimated teleosts that may also be facilitated by paCA. Thus, to create experimental contrasts in tissue O 2 extraction, Atlantic salmon were acclimated to normoxia or hypoxia (40% air saturation for more than six weeks), and the role of paCA in enhancing tissue O 2 extraction was tested by inhibiting paCA at rest and during submaximal exercise. Our results show that: (i) in both acclimation groups, the inhibition of paCA increased cardiac output by one-third, indicating a role of paCA in promoting tissue O 2 extraction during exercise, recovery and at rest; (ii) the recruitment of paCA was plastic and increased following hypoxic acclimation; and (iii) maximal exercise performance in salmon, and thus a successful spawning migration, may not be possible without paCA.
Respiration Physiology, 1987
The effects of haemoglobin-oxygen affinity and of cooperativity in oxygen binding on the oxygen extraction and ventilation requirement in fish are analysed using the mathematical model of Malte and Weber (1985). It is shown that a high affinity may allow a substantial reduction in ventilatory requirement and that optimal 02 uptake depends on a delicate balance between affinity and cooperativity. Using Pso and n H values from the literature, the oxygen extraction values predicted by the model for carp and rainbow trout coincide neatly with the values found for these species, indicating that the differences in oxygen extraction are a direct result of different blood oxygen binding properties. Extraction; Mathematical model; Oxygen affinity; Ventilation requirement The efficacy of oxygen extraction from water at the respiratory surfaces varies greatly among fishes, with values ranging from less than 50~o in rainbow trout (Cameron and Davis, 1970; Davis and Cameron, 1971) to more than 80~o in carp (Lomholdt and Johansen, 1979). Differences in extraction reflect differences in ventilation-perfusion ratio for a given arterio-venous oxygen content difference. This is illustrated by combining the mass balances for water and blood (see Materials and methods for explanation of symbols): 1Vlo2 = ~'w. ~w(PIo2-PEo2) = "~rb(Cao2-CVo2) Vw _ (Cao~-Cvo2). PIo2 _ Cao~-CVo~ 1 '~b ~w(PIo2-PEo2) PIo2 CIo2 ew A reduced Vw/'(Po, all else being constant, is tantamount to reduced oxygen loading in the gill (cf Piiper and Scheid, 1975; Malte and Weber, 1985). If the arterio-venous
Journal of Experimental Biology, 2013
It 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 6week period of moderate hypoxia exposure (10.2-12.1kPa P O2 , 21±1°C) and compared with those of normoxic controls (P O2 =20-21kPa, 21±1°C). The critical oxygen pressure (P crit ) limit of both groups was unchanged at ~7kPa, 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±1.1kPa) 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.
Journal of Great Lakes Research, 2004
We present the first measurements of routine oxygen uptake (VO 2 ) of the bloater (Coregonus hoyi), including the effects of temperature and hydrostatic pressure. For temperature experiments, ten 24 hour trials were conducted each at 10.5°C and 7°C, using flow-through respirometry. Average routine VO 2 was approximately 130 mg O 2 /(kg*hr) at 10.5°C and approximately 120 mg O 2 /(kg*hr) at 7°C. These values did not differ significantly, probably because we used temperatures spanning the thermal range of bloater, within which this species may conserve routine metabolism. Derivations of daily food ration for bloater were calculated and compared with a previous bioenergetics model. For pressure experiments, the diel vertical migrations bloater undertake in the wild were simulated using a flowthrough respirometer that could be pressurized. Ten 3-day trials were conducted, consisting of an overnight acclimation to the respirometer, a 12-hour pressure regime, and a day of recovery. The pressure regime involved a compression from 1 atm (atmospheric pressure) to 4 atm over 6 hours and a subsequent decompression of the same magnitude and duration. Increases in hydrostatic pressure elicited a rise in bloater VO 2 and motor activity; conversely, the subsequent decrease in hydrostatic pressure caused a return of oxygen uptake and motor activity to baseline values at 1 atm. We hypothesize that pressure-induced compression of the gas bladder explain the changes in VO 2 , because increased swimming (causing increased VO 2 ) is needed to maintain station when the swimbladder is compressed.
The problem of understanding the effect of the environment on fish activities and performance, in any generalized way, remains intractable. Solving this issue is, however, a key to addressing contemporary environmental concerns. As suggested 20 years ago by W. H. Neill, the authors returned to the drawing board, using as a background the conceptual scheme initially proposed by F. E. J. Fry. They revisited the effect of ambient oxygen availability upon fish metabolism and clarified the definitions of limiting, critical and incipient lethal oxygen (ILO) levels. The concepts of oxy-conformer and oxy-regulator are revisited, and P. W. Hochachka's idea of scope for survival is explored. Finally, how the cardiovascular system contributes to the capacity of fishes to respond to the reduced oxygen availability is considered. Various hands-on recommendations and software (R scripts) are provided for researchers interested in investigating these concepts.
Comparative biochemistry and physiology. A, Comparative physiology, 1985
The oxygen consumption of rat versus turtle brain and heart slices was compared as a function of extracellular pH and temperature. At pH = 6.20 rat (mammalian) brain and heart slices show a significant depression of oxygen consumption as compared to pH = 7.50 at temperatures of both 24 degrees and 37 degrees C. In the turtle oxygen consumption in brain and heart slices was not depressed at pH = 6.20 compared to pH = 7.50 at 24 degrees C and brain oxygen consumption was not significantly different at the two pH values at 37 degrees C. Turtle heart QO2 was depressed at 37 degrees C. The results suggest that extracellular acidosis depresses mitochondrial O2 uptake in mammalian brain and heart, playing a role in the bioenergetic manifestations of O2 depletion. Turtle brain mitochondria do not show a depression of QO2 at the acidotic pH. The resistance to acidosis of turtle brain mitochondria presumably enhances the possibility of survival following prolonged diving by maintaining ATP ge...