Differential responses in ammonia excretion, sodium fluxes and gill permeability explain different sensitivities to acute high environmental ammonia in three freshwater teleosts

Hon Jung Liew, Amit Kumar Sinha, C. Michele Nawata, Ronny Blust, Chris M. Wood, Gudrun De Boeck

Research output: Contribution to journalArticle

37 Scopus citations

Abstract

We examined the acute physiological responses to high environmental ammonia (HEA), particularly the linkages between branchial ammonia fluxes and unidirectional Na+ fluxes, as well as urea excretion, cortisol, and indicators of gill permeability in three freshwater teleosts differing in their sensitivities to ammonia; the highly sensitive salmonid Oncorhynchus mykiss (rainbow trout), the less sensitive cyprinid Cyprinus carpio (common carp) and the highly resistant cyprinid Carassius auratus (goldfish). Fish were acutely exposed to two sub-lethal ammonia concentrations (as NH4HCO3) at pH 7.9: 1mM for a period of 12h, identical for all species, and 5mM for the cyprinids and 1.4mM for the trout for 3h. Elevation of plasma cortisol at both levels of HEA was apparent in all species. At 1mM, ammonia excretion (Jamm) was inhibited to a greater extent in trout than cyprinids and concurrently a significantly higher plasma ammonia level was evident in trout. However Jamm was reversed in all species at 5 or 1.4mM. Goldfish showed a significant increase in urea excretion rate (Jurea) during HEA exposure. In carp and trout, neither level of HEA elevated Jurea but urea production was increased as evidenced by a considerable elevation of plasma urea. At 1mM HEA, Na+ imbalance became progressively more severe in trout and carp due to a stimulation of unidirectional Na+ efflux (JoutNa) without a concomitant increase in unidirectional Na+ influx (JinNa). Additionally, a transient reduction of JinNa was evident in trout. Goldfish showed an opposite trend for JoutNa with reduced efflux rates and a positive Na+ balance during the first few hours of HEA. However, after 12h of exposure, both JinNa and JoutNa were also increased in both carp and goldfish, whereas only JoutNa was increased in trout, leading to a net Na+ loss. Na+ homeostasis was entirely disrupted in all three species when subjected to the 5 or 1.4mM ammonia for 3h: JinNa was significantly inhibited while considerable activation of JoutNa was observed. Diffusive water efflux rates and net K+ loss rates across the gills were enhanced during HEA only in trout, indicating an increment in gill transcellular permeability. Transepithelial potential was increased in all the species during ammonia exposure, but to the least extent in goldfish. Overall, for several different physiological systems, trout were most disturbed, and goldfish were least disturbed by HEA, helping to explain the differential ammonia tolerance of the three species.

Original languageEnglish (US)
Pages (from-to)63-76
Number of pages14
JournalAquatic Toxicology
Volume126
DOIs
StatePublished - Jan 5 2013

Keywords

  • Ammonia excretion
  • Common carp
  • Gill permeability
  • Goldfish
  • High environmental ammonia (HEA)
  • Rainbow trout
  • Sodium flux
  • Transepithelial potential
  • Urea excretion

ASJC Scopus subject areas

  • Aquatic Science
  • Health, Toxicology and Mutagenesis

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