Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): new angles to the osmorespiratory compromise

Abstract

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.

Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus (Agassiz)

“…Regrettably, we did not measure ventilation rates or gill perfusion. Therefore, we cannot conclude whether the increased Ṁ O2 was related to increased water and/or blood flow, which would aggravate the osmorespiratory compromise (Wood et al, 2009), or whether it was caused by an increased oxygen demand and improved diffusion.…”

“…Ventilation does increase under hypoxia (Chippari-Gomes et al, 2005; Scott et al, 2008), which puts the fish at risk of losing more ions to their extremely dilute environment due to the osmo-respiratory compromise (Randall et al, 1972;Nilsson, 2007). However, previous research has shown that under these circumstances oscars are capable of reducing their net ion losses efficiently, thereby decreasing the need for active ion uptake (Wood et al, 2007;Wood et al, 2009). Because branchial ionoregulation is an energetically demanding process responsible for 2-20% of the energy metabolism (Febry and Lutz, 1987), it is important to reduce this cost as much as possible under hypoxic or anoxic conditions; correspondingly, activities of gill and kidney Na + /K + -ATPases are substantially reduced under severe hypoxia (Richards et al, 2007;Wood et al, 2007).…”

Nitric oxide metabolites in goldfish under normoxic and hypoxic conditions

“…In addition to these explanations, it should also be considered whether an enhanced urinary excretion or efflux via the gills might contribute to lower extracellular nitrite and nitrate in hypoxia. A recent study on goldfish, however, showed that hypoxia actually inhibits passive branchial ion efflux in spite of an increased respiratory surface area of the gills (Mitrovic et al, 2009), and in another hypoxia-tolerant fish (Amazonian oscar), both urinary and branchial ion excretion rates were decreased rather than increased by hypoxia (Wood et al, 2009).…”

Measuring gill paracellular permeability with polyethelene glycol-4000 in freely swimming trout: proof of principle

“…hypoxia (Wood et al, 2009) found no change in branchial permeability (measured in the efflux direction) to polyethylene glycol MW-4000 [PEG-4000, a classic gill paracellular marker (e.g. Wood and Part, 1997;Chasiotis and Kelly, 2011)].…”