Rapid regulation of Na⁺fluxes and ammonia excretion in response to acute environmental hypoxia in the Amazonian oscar,Astronotus ocellatus

Abstract

The Amazonian oscar is extremely resistant to hypoxia, and tolerance scales with size. Overall, ionoregulatory responses of small (ϳ15 g) and large oscars (ϳ200 g) to hypoxia were qualitatively similar, but the latter were more effective. Large oscars exhibited a rapid reduction in unidirectional Na ϩ uptake rate at the gills during acute hypoxia (PO2 ϳ10 mmHg), which intensified with time (7 or 8 h); Na ϩ efflux rates were also reduced, so net balance was little affected. The inhibitions were virtually immediate (1st h) and preceded a later 60% reduction (at 3 h) in gill Na ϩ -K ϩ -ATPase activity, reflected in a 60% reduction in maximum Na ϩ uptake capacity without change in affinity (Km) for Na ϩ . Upon acute restoration of normoxia, recovery of Na ϩ uptake was delayed for 1 h. These data suggest that dual mechanisms may be involved (e.g., immediate effects of O 2 availability on transporters, channels, or permeability, slower effects of Na ϩ -K ϩ -ATPase regulation). Ammonia excretion appeared to be linked indirectly to Na ϩ uptake, exhibiting a Michaelis-Menten relationship with external [Na ϩ ], but the Km was less than for Na ϩ uptake. During hypoxia, ammonia excretion fell in a similar manner to Na ϩ fluxes, with a delayed recovery upon normoxia restoration, but the relationship with [Na ϩ ] was blocked. Reductions in ammonia excretion were greater than in urea excretion. Plasma ammonia rose moderately over 3 h hypoxia, suggesting that inhibition of excretion was greater than inhibition of ammonia production. Overall, the oscar maintains excellent homeostasis of ionoregulation and N-balance during severe hypoxia. teleost fish; ionoregulation; nitrogen metabolism; sodium-potassiumATPase; ion channels THE PRESENT STUDY USES the hypoxia-tolerant oscar (acará-açu; Astronotus ocellatus), an entirely water-breathing Amazonian cichlid, to examine the effects of low environmental O 2 on two key aspects of gill function, ionoregulation and nitrogenous waste excretion. The oscar commonly encounters hypoxia in its natural environment when it enters the seasonally flooded jungle to feed and reproduce; adults are reported to survive up to 6 h of complete anoxia and can tolerate levels of 5-20% air saturation for 20 -50 h (1, 2, 32). There are several reasons for believing that ionic balance and ammonia excretion may be particularly sensitive to hypoxia in freshwater fish, but to date, these areas have received little experimental attention.First, the respiratory-osmoregulatory compromise at the gills has been well documented in exercise studies on several teleost species: the effective gill area and diffusion distance are adjusted as a trade-off between providing the permeability required for gas exchange, while minimizing diffusive ion losses and osmotic water gain (12, 13, 57, 58). During environmental hypoxia, it is probable that similar lamellar recruitment and decreased diffusion distance occurs to help sustain O 2 uptake (17, 18) because gill O 2 transfer factor, an index of effective O 2 permeability, increase...

Metabolic fates and effects of nitrite in brown trout under normoxic and hypoxic conditions: blood and tissue nitrite metabolism and interactions with branchialNOS,Na+/K+-ATPaseandhsp70expression

“…The relative short exposure time (24 h) could also be important. Earlier reports of a decreased branchial NKA activity during hypoxia used either stronger hypoxia and/or longer exposures (Richards et al, 2007;Wood et al, 2007;Lundgreen et al, 2008;Hansen and Jensen, 2010). Indeed, shortterm (4 h) hypoxia at a water P O2 of 80 mmHg did not change gill NKA activity in rainbow trout (Iftikar et al, 2010) as we show here for brown trout.…”

“…Hypoxia per se can also decrease gill NKA activity in fish (Richards et al, 2007;Wood et al, 2007;Lundgreen et al, 2008;Hansen and Jensen, 2010). It was therefore unexpected that neither nitrite nor hypoxia changed NKA activity in the present experiments (Fig.…”

Responses to hypoxia and recovery: repayment of oxygen debt is not associated with compensatory protein synthesis in the Amazonian cichlid,Astronotus ocellatus

“…Recent studies have begun investigation into the various ATP-consuming processes that contribute to the whole animal metabolic depression. These studies have shown significant reduction in Na + ,K + -ATPase in gill and kidney during hypoxia exposure (Richards et al, 2007) which is accompanied by a reduction of ion exchange at the gills and an overall reduction in metabolic nitrogenous waste production (urea and ammonia) (Wood et al, 2007). The decrease in these ATP consuming processes are not accompanied by changes in concentration of ATP (Richards et al, 2007), indicating that A. ocellatus is able to successfully tolerate extended hypoxia exposure because of the reduction in key ATP-consuming processes.…”

The effects of hypoxia on active ionic transport processes in the gill epithelium of hyperregulating crab, Carcinus maneas

“…We have demonstrated a small decrease of conductance under severe 1.6 mg O 2 hypoxia, when > 95% of Isc was inhibited by hypoxia. The decreased conductance of the posterior gill epithelium in DSW reduces loss of salts in Carcinus and this may lead to a lesser expense of energy, as found in fish gills (Wood et al, 2007(Wood et al, , 2009. Such a decreased conductance might be advantageous for osmoregulation under severe hypoxia in DSW.…”

“…Upon reoxygenation Na + uptake was recovered. The low branchial paracellular permeability tested during swimming exercise may be an additional adaptive mechanism in limiting osmoregulatory cost under hypoxia (Wood et al, 2007;Robertson et al, 2015). Hypoxia diminishes intracellular ATP production in the trout hepatocytes (Bogdanova et al, 2005).…”