Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys

Abstract

In the 1930s, August Krogh, Homer Smith, and Ancel Keys knew that teleost fishes were hyperosmotic to fresh water and hyposmotic to seawater, and, therefore, they were potentially salt depleted and dehydrated, respectively. Their seminal studies demonstrated that freshwater teleosts extract NaCl from the environment, while marine teleosts ingest seawater, absorb intestinal water by absorbing NaCl, and excrete the excess salt via gill transport mechanisms. During the past 70 years, their research descendents have used chemical, radioisotopic, pharmacological, cellular, and molecular techniques to further characterize the gill transport mechanisms and begin to study the signaling molecules that modulate these processes. The cellular site for these transport pathways was first described by Keys and is now known as the mitochondrion-rich cell (MRC). The model for NaCl secretion by the marine MRC is well supported, but the model for NaCl uptake by freshwater MRC is more unsettled. Importantly, these ionic uptake mechanisms also appear to be expressed in the marine gill MRC, for acid-base regulation. A large suite of potential endocrine control mechanisms have been identified, and recent evidence suggests that paracrines such as endothelin, nitric oxide, and prostaglandins might also control MRC function.

Assessing causation of the extirpation of stream macroinvertebrates by a mixture of ions

“…The Watershed Assessment Database (WABbase), which was obtained from the West Virginia Department of Environmental Protection, is described by Cormier et al [1] and was used to derive the conductivity benchmark. Additional information sources were used, including (1) toxicity tests from peer-reviewed literature [7]; (2) information on the effects of ionic mixtures on freshwater invertebrates from standard texts and physiological reviews [8][9][10][11][15][16][17][18][19][20][21][22][23]; (3) a U.S. Environmental Protection Agency (U.S. EPA) Region 3 data set from Gregory J. Pond, which includes the original data found in Pond et al [6] and data collected for a Programmatic Environmental Impact Assessment [24]; (4) data on the composition of Marcellus shale brine from Amy Bergdale, U.S. EPA Region 3, based on analyses by drilling operators; (5) data from the Kentucky Division of Water database [2]; and (6) geographic and related information from the West Virginia Department of Environmental Protection and public sources [1,2].…”

“…Aqueous salts are dissolved ions that are readily available for uptake by aquatic organisms as they pass over their respiratory and other permeable surfaces [8,9,11,17,20,[41][42][43]. Benthic invertebrates that inhabit naturally low-conductivity streams (Table 1) may be subjected to waters that have a greater concentration of ions due to local effluents [2,7].…”

“…Scoring-Evidence of a mechanism of exposure is from knowledge that the ions are present in streams [2,7] and from general knowledge of animal physiology and the anatomy of insects and other aquatic invertebrates [8,9,11,17,20,[41][42][43] (þ). Because the exposure is by the same mechanism that provides respiration (i.e., maintenance of water flow over permeable membranes), it is strong (þ).…”

“…Maintaining homeostasis involves osmotic and ionic regulation by cells and tissues. Freshwater organisms, including mayflies, are known to use various physical structures and physiological mechanisms to maintain water content, charge balance, and specific ionic concentrations [8,9,11,17,20,21,[41][42][43]. Many freshwater invertebrates, including mayflies, have mitochondrion-rich chloride cells on gills and other surfaces that take up chloride and other ions [11,17].…”

“…Our analysis uses general knowledge from laboratory experiments and also field observations from streams in Appalachia. Although the effects of elevated ionic concentration on freshwater organisms are well established, most studies have focused on Na þ and Cl À , which are associated with marine ecosystems or salts from marine deposits [8][9][10][11]. However, ionic constituents can be quite different when land disturbance increases ionic concentration.…”