Mechanisms of ion transport inPotamotrygon, a stenohaline freshwater elasmobranch native to the ion-poor blackwaters of the Rio Negro

Abstract

SUMMARYStingrays of the family Potamotrygonidae are the only stenohaline freshwater elasmobranchs. Potomotrygon sp. collected from the ion-poor blackwaters ([Na+], [Cl-] and[Ca2+]=10-30 μmol l-1, pH 6.1) of the Rio Negro,Amazonas, Brazil, were ammoniotelic (91% ammonia-N, 9% urea-N excretion) and exhibited blood chemistry (Na+, Cl-, urea, ammonia and glucose levels and osmolality) typical of freshwater teleosts. Unidirectional Na+ and Cl- influx rates, measured with radiotracers,displayed saturation kinetics. The relationships for Cl- and Na+ had similar Km values (300-500 μmol l-1), but Jmax values for Cl-(approximately 950 μmol kg-1 h-1) were almost twice those for Na+ (approximately 500 μmol kg-1h-1). Cl- efflux rates varied with external concentration, but Na+ efflux rates did not. There were no differences in the kinetic variables (Km, Jmax) for influx between animals acclimated to their native ion-poor blackwater or to ion-rich hard water, but efflux rates for both Na+ and Cl- were lower in the former, yielding much lower balance points (external Na+ or Cl- levels at which influx and efflux were equal). Na+, Cl- and Ca2+ uptake were all strongly inhibited by acute exposure to pH 4.0, but efflux rates and Ca2+ binding to the body surface did not change. Na+ influx was inhibited by amiloride (10-4 mol l-1) and by two of its analogs, phenamil (4×10-5mol l-1) and HMA (4×10-5 mol l-1), with the latter being slightly more potent, while Cl- fluxes were unaffected. Cl- fluxes were insensitive to DIDS(2×10-5 mol l-1 or 10-4 mol l-1) and SITS (10-4 mol l-1), but both influx and efflux rates were strongly inhibited by DPC (10-4 mol l-1) and thiocyanate (10-4 mol l-1). Ammonia excretion was unresponsive to large changes in water Na+concentration, but was elevated by 70% during acute exposure to pH 4.0 and transiently inhibited by approximately 50% by amiloride and its analogues. The strategy of adaptation to ion-poor blackwater appears similar to that of some Rio Negro teleosts (Cichlidae) in which low-affinity transport systems are relatively sensitive to inhibition by low pH but are complemented by low diffusive loss rates. Ionic transport systems in these freshwater elasmobranchs, although superficially similar to those in some freshwater teleosts, may bear more resemblance to their presumed evolutionary precursors in marine elasmobranchs.

Hematology, biochemical profile and thyroid hormones of four species of freshwater stingrays of the genus Potamotrygon

“…However, sodium levels were similar with Potamotrygon spp. (164 ± 5.6 mmol.L -1 ), P. magdalenae (141 ± 2.4 mmol.L -1 ) and Potamotrygon sp (178,2 ± 4.8 mmol.L -1 ) (WOOD et al, 2002;CAIN;HARMS;SEGARS, 2004;ROBINSON, 2010). Chlorine and potassium was also similar with P. magdalenae (147 ± 4.5 and 8,5 ± 0.29 mmol.L -1 ) (OGAWA; HIRANO, 1982), but calcium level was higher (3 ± 0.09 mg.dL -1 ).…”

“…The absence of eosinophils in P. scobina could be physiological, as well as in teleost fish generally there is great variation in their blood percentage (TAVARES-DIAS; MORAES, 2004). Wood et al (2002) showed that Potamotrygonidae family presents characteristics of both freshwater and marine fish, based on the study of sodium and chloride exchange and urea excretion in Potamotrygon hystrix and Potamotrygon thorsoni. Emery (1986) associated the low metabolic activity of these fish with the low rates of ion exchanges in this family, which was also observed in this work.…”

“…Chlorine, sodium, and calcium levels of the Potamotrygon species evaluated in our study were lower than shark serum levels (STOSKOPF, 1993), likely due to the saltwater habitat of the sharks. Potamotrygonidae fish have an adaptation to low ionic water similar to freshwater bony fishes, with a low affinity ionic transport system (WOOD et al, 2002;ROBINSON, 2010).…”

Hematological and plasma biochemical profile of two species of freshwater stingrays from the Amazon

“…Furthermore, the work present in the literature with freshwater stingrays in natural environments was carried out mainly in black water environments in the Negro River basin, Amazonas (Brito et Wood et al 2002), and to date, there are no studies on the determination of hematological reference intervals for stingrays from white water environments in the Amazon hydrographic basin.…”

Fish-microbe systems in the hostile but highly biodiverse Amazonian blackwaters

“…Campbell et al ., (1997) demonstrated, by transmission electron microscopy, that DOC molecules can bind directly to the surface of gill cells. In fish exposed to acidic waters, DOC mitigates the inhibition of Na + uptake and ammonia excretion (Wood et al , 2003; Al-Reasi et al , 2016;), lowers the transepithelial potential (TEP) (Galvez et al , 2008), protects against the elevation of diffusive Na + and Cl − loss (Wood et al , 2002, 2003; Gonzalez et al , 2002, 2006; Al-Reasi et al , 2016; Duarte et al , 2016, 2018) and reduces the gill binding and toxicity of metals (Wood et al ., 2011; Cremazy et al ., 2016; Duarte et al ., 2021). Humic DOC has also been shown to significantly decrease respiratory stress caused by exposure to low pH and increase survival of fish at pH 4 (Holland et al ., 2014b).…”