SUMMARYEarlier studies demonstrated that oscars, endemic to ion-poor Amazonian waters, are extremely hypoxia tolerant, and exhibit a marked reduction in active unidirectional Na + uptake rate (measured directly) but unchanged net Na + balance during acute exposure to low P O2 , indicating a comparable reduction in whole body Na + efflux rate. However, branchial O 2 transfer factor does not fall. The present study focused on the nature of the efflux reduction in the face of maintained gill O 2 permeability. Direct measurements of 22 Na appearance in the water from bladder-catheterized fish confirmed a rapid 55% fall in unidirectional Na + efflux rate across the gills upon acute exposure to hypoxia (P O2 =10-20 torr; 1 torr=133.3 Pa), which was quickly reversed upon return to normoxia. An exchange diffusion mechanism for Na + is not present, so the reduction in efflux was not directly linked to the reduction in Na + influx. A quickly developing bradycardia occurred during hypoxia. Transepithelial potential, which was sensitive to water [Ca 2+ ], became markedly less negative during hypoxia and was restored upon return to normoxia. Ammonia excretion, net K + loss rates, and 3 H 2 O exchange rates (diffusive water efflux rates) across the gills fell by 55-75% during hypoxia, with recovery during normoxia. Osmotic permeability to water also declined, but the fall (30%) was less than that in diffusive water permeability (70%). In total, these observations indicate a reduction in gill transcellular permeability during hypoxia, a conclusion supported by unchanged branchial efflux rates of the paracellular marker [ 3 H]PEG-4000 during hypoxia and normoxic recovery. At the kidney, glomerular filtration rate, urine flow rate, and tubular Na + reabsorption rate fell in parallel by 70% during hypoxia, facilitating additional reductions in costs and in urinary Na + , K + and ammonia excretion rates. Scanning electron microscopy of the gill epithelium revealed no remodelling at a macro-level, but pronounced changes in surface morphology. Under normoxia, mitochondria-rich cells were exposed only through small apical crypts, and these decreased in number by 47% and in individual area by 65% during 3 h hypoxia. We suggest that a rapid closure of transcellular channels, perhaps effected by pavement cell coverage of the crypts, allows conservation of ions and reduction of ionoregulatory costs without compromise of O 2 exchange capacity during acute hypoxia, a response very different from the traditional osmorespiratory compromise.
SUMMARY The transition from aquatic to aerial respiration is associated with dramatic physiological changes in relation to gas exchange, ion regulation,acid–base balance and nitrogenous waste excretion. Arapaima gigas is one of the most obligate extant air-breathing fishes,representing a remarkable model system to investigate (1) how the transition from aquatic to aerial respiration affects gill design and (2) the relocation of physiological processes from the gills to the kidney during the evolution of air-breathing. Arapaima gigas undergoes a transition from water-to air-breathing during development, resulting in striking changes in gill morphology. In small fish (10 g), the gills are qualitatively similar in appearance to another closely related water-breathing fish (Osteoglossum bicirrhosum); however, as fish grow (100–1000 g), the inter-lamellar spaces become filled with cells, including mitochondria-rich(MR) cells, leaving only column-shaped filaments. At this stage, there is a high density of MR cells and strong immunolocalization of Na+/K+-ATPase along the outer cell layer of the gill filament. Despite the greatly reduced overall gill surface area, which is typical of obligate air-breathing fish, the gills may remain an important site for ionoregulation and acid–base regulation. The kidney is greatly enlarged in A. gigas relative to that in O. bicirrhosum and may comprise a significant pathway for nitrogenous waste excretion. Quantification of the physiological role of the gill and the kidney in A. gigas during development and in adults will yield important insights into developmental physiology and the evolution of air-breathing.
SUMMARYGoldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3·mg·O 2 ·l -1 ) for 24·h followed by 12·h recovery in normoxic water (6·mg·O 2 ·l -1 at 3200·m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8·h of hypoxia and almost complete by 24·h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water-blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24·h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na
SUMMARYThe salinity tolerance of the `California' Mozambique tilapia(Oreochromis mossambicus × O. urolepis hornorum), a current inhabitant of the hypersaline Salton Sea in California, USA, was investigated to identify osmoregulatory stress indicators for possible use in developing a model of salinity tolerance. Seawater-acclimated (35 g l–1) tilapia hybrids were exposed to salinities from 35–95 g l–1, using gradual and direct transfer protocols, and physiological (plasma osmolality, [Na+],[Cl–], oxygen consumption, drinking rate, hematocrit, mean cell hemoglobin concentration, and muscle water content), biochemical(Na+, K+-ATPase) and morphological (number of mature,accessory, immature and apoptotic chloride cells) indicators of osmoregulatory stress were measured. Tilapia tolerated salinities ranging from 35 g l–1 to 65 g l–1 with little or no change in osmoregulatory status; however, in fish exposed to 75–95 g l–1 salinity, plasma osmolality, [Na+],[Cl–], Na+, K+-ATPase, and the number of apoptotic chloride cells, all showed increases. The increase in apoptotic chloride cells at salinities greater than 55 g l–1, prior to changes in physiological and biochemical parameters, indicates that it may be the most sensitive indicator of osmoregulatory stress. Oxygen consumption decreased with salinity, indicating a reduction in activity level at high salinity. Finally, `California' Mozambique tilapia have a salinity tolerance similar to that of pure Mozambique tilapia; however, cellular necrosis at 95 g l–1 indicates they may be unable to withstand extreme salinities for extended periods of time.
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...
Soon after hatching, the osteoglossid fish Arapaima gigas undergoes a rapid transition from a water breather to an obligate air breather. This is followed by a gradual disappearance of gill lamellae, which leaves smooth filaments with a reduced branchial diffusion capacity due to loss of surface area, and a fourfold increase in diffusion distance. This study evaluated the effects these changes have on gill function by examining two size classes of fish that differ in gill morphology. In comparison to smaller fish (approximately 67.5 g), which still have lamellae, larger fish (approximately 724.2 g) without lamellae took up a slightly greater percentage of O2 across the gills (30.1% vs. 23.9%), which indicates that the morphological changes do not place limitations on O2 uptake in larger fish. Both size groups excreted similar percentages of CO2 across the gills (85%-90%). However, larger fish had higher blood PCO2 (26.51.9 vs. 16.51.5 mmHg) and HCO3(-) (40.2 +/- 2.9 vs. 33.6 +/- 4.5 mmol L(-1)) concentrations and lower blood pH (7.58 +/- 0.01 vs. 7.70 +/- 0.04) than did smaller fish, despite having lower mass-specific metabolisms, suggesting a possible diffusion limitation for CO2 excretion in larger fish. With regard to ion regulation, rates of diffusive Na+ loss were about 3.5 times higher in larger fish than they were in smaller fish, despite the lowered branchial diffusion capacity, and rates of Na+ uptake were higher by about the same amount despite 40% lower activity of branchial Na+/K+-ATPase. Kinetic analysis of Na uptake revealed an extremely low-affinity (K(m) = 587.9 +/- 169.5 micromol L(-1)), low-capacity (J(max) = 265.7 +/- 56.8 nmol g(-1) h(-1)) transport system. These data may reflect a general reduction in the role of the gills in ion balance. Renal Na+/K+-ATPase activity was 5-10 times higher than Na+/K+-ATPase activity in the gills, and urine: plasma ratios for Na+ and Cl(-) were very low (0.001-0.005) relative to that of other fish, which suggested an increased role for dietary salt intake and renal salt retention and which was representative of a more "terrestrial" mode of ion regulation. Such de-emphasis of branchial ion regulation confers greatly reduced sensitivity of diffusive ion loss to low water pH. Ammonia excretion also appeared to be impacted by gill changes. Rates of ammonia excretion in larger fish were one third less than that in smaller fish, despite larger fish having blood ammonia concentrations that were twice as high.
The gills of many fish, but in particular those of crucian carp (Carassius carassius) and goldfish (Carassius auratus), are capable of extensive remodeling in response to changes in oxygen (O2), temperature, and exercise. In this study, we investigated the interspecific variation in hypoxia-induced gill modeling and hypoxia tolerance in 10 closely related groups of cyprinids (nine species, with two strains of Cyprinus carpio). There was significant variation in hypoxia tolerance, measured as the O2 tension (P(O2)) at which fish lost equilibrium (LOEcrit), among the 10 groups of carp. In normoxia, there was a significant, phylogenetically independent relationship between mass-specific gill surface area and LOEcrit, with the more hypoxia-tolerant carp having smaller gills than their less hypoxia-tolerant relatives. All groups of carp, except the Chinese bream (Megalobrama pellegrini), increased mass-specific gill surface area in response to 48 h of exposure to hypoxia (0.7 kPa) through reductions in the interlamellar cell mass (ILCM) volume. The magnitude of the hypoxia-induced reduction in the ILCM was negatively correlated with LOEcrit (and thus positively correlated with hypoxia tolerance), independent of phylogeny. The hypoxia-induced changes in gill morphology resulted in reduced variation in mass-specific gill surface area among species and eliminated the relationship between LOEcrit and mass-specific gill surface area. While behavioral responses to hypoxia differed among the carp groups, there were no significant relationships between hypoxia tolerance and the Po2 at which aquatic surface respiration (ASR) was initiated or the total number of ASR events observed during progressive hypoxia. Our results are the first to show that the extent of gill remodeling in cyprinids is associated with hypoxia tolerance in a phylogenetically independent fashion.
We utilized the rainbow trout, a hypoxia-intolerant freshwater teleost, to examine ionoregulatory changes at the gills during hypoxia. Progressive mild hypoxia led first to a significant elevation (by 21%) in J(Na)(influx) (measured with 22Na), but at 4-h hypoxia when PCO2 reached approximately 110 mmHg, there was a 79% depression in J(Na)(influx). Influx remained depressed during the first hour of normoxic recovery but was restored back to control rates thereafter; there were no significant changes in J(Na)(efflux) or J(Na)(net). A more prolonged (8 h) and severe hypoxic (approximately 80 mmHg) exposure induced a triphasic response whereby J(Na)(influx) was significantly elevated during the first hour, as during mild hypoxia, but returned to control rates during the subsequent 3 h. Thereafter, rates started to gradually increase and remained significantly elevated by about 38% through to 8 h of hypoxia. A similar triphasic trend was observed with J(Na)(efflux) but with larger changes than in J(Na)(influx), such that negative Na+ balance occurred during the hypoxic exposure. Net K+ loss rates to the water approximately doubled. There were no significant alterations in ammonia excretion rates in either of the hypoxia regimes. Branchial Na+/K+-ATPase activity did not change during 4 h at PO2 approximately 80 mmHg or return to normoxia; H+-ATPase activity also did not change during hypoxia but was significantly depressed by approximately 75% after 6 h of normoxic recovery. Scanning electron microscopy revealed that within 1 h of exposure to PO2 approximately 80 mmHg, exposed mitochondria-rich cell (MRC) numbers increased by 30%, while individual MRC exposed surface area and total MRC surface area both increased by three- to fourfold. MRC numbers had decreased below control levels by 4 h of hypoxia, but surface exposure remained elevated by approximately twofold, a response that persisted through 6 h of normoxic recovery. Environmental hypoxia induces complex changes in gill ionoregulatory function in this hypoxia-intolerant species that are very different from those recently reported in the hypoxia-tolerant Amazonian oscar.
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