The potential for salt toxicity: Can the trans-epithelial potential (TEP) across the gills serve as a metric for major ion toxicity in fish?

Chris M. Wood; M. Danielle McDonald; Martin Grosell; David R. Mount; William J. Adams; Beverly H.K. Po; Kevin V. Brix

doi:10.1016/j.aquatox.2020.105568

The potential for salt toxicity: Can the trans-epithelial potential (TEP) across the gills serve as a metric for major ion toxicity in fish?

Chris M. Wood, M. Danielle McDonald, Martin Grosell, David R. Mount, William J. Adams, Beverly H.K. Po, Kevin V. Brix

Research output: Contribution to journal › Article › peer-review

11 Scopus citations

Abstract

An emerging Multi-Ion Toxicity (MIT) model for assessment of environmental salt pollution is based on the premise that major ion toxicity to aquatic organisms is related to a critical disturbance of the trans-epithelial potential across the gills (ΔTEP), which can be predicted by electrochemical theory. However, the model has never been evaluated physiologically. We directly tested key assumptions by examining the individual effects of eight different salts (NaCl, Na₂SO₄, MgCl₂, MgSO₄, KCl, K₂SO₄, CaCl₂, and CaSO₄) on measured TEP in three different fish species (fathead minnow, Pimephales promelas = FHM; channel catfish, Ictalurus punctatus = CC; bluegill, Lepomis macrochirus = BG). A geometric concentration series based on previously reported 96-h LC50 values for FHM was used. All salts caused concentration-dependent increases in TEP to less negative/more positive values in a pattern well-described by the Michaelis-Menten equation. The ΔTEP responses for different salts were similar to one another within each species when concentrations were expressed as a percentage of the FHM LC50. A plateau was reached at or before 100 % of the LC50 where the ΔTEP values were remarkably consistent, with only 1.4 to 2.2-fold variation. This relative uniformity in the ΔTEP responses contrasts with 28-fold variation in salt concentration (in mmol L⁻¹), 9.6-fold in total dissolved solids, and 7.9-fold in conductivity at the LC50. The Michaelis-Menten Km values (salt concentrations causing 50 % of the ΔTEP_max) were positively related to the 96-h LC50 values. ΔTEP responses were not a direct effect of osmolarity in all species and were related to specific cation rather than specific anion concentrations in FHM. These responses were stable for up to 24 h in CC. The results provide strong physiological support for the assumptions of the MIT model, are coherent with electrochemical theory, and point to areas for future research.

Original language	English (US)
Article number	105568
Journal	Aquatic Toxicology
Volume	226
DOIs	https://doi.org/10.1016/j.aquatox.2020.105568
State	Published - Sep 2020
Externally published	Yes

Bibliographical note

Funding Information:
We are grateful to Rio Tinto for critical seed funding for this work. Additional funding was provided by Ecotox, a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant ( RGPIN-2017-03843 ) to CMW, by an EPRI contract ( 10009699 ) to CMW, and a National Science Foundation grant ( IOS-1754550 ) to MDM. MG is a Maytag Professor of Ichthyology. We thank John Goodrich-Mahoney and Jeff Thomas of EPRI for valuable advice and co-ordination, Dr. Russ Erickson of US EPA for important input, Dr. Markus Hecker of the University of Saskatchewan for fathead minnow supply, Dr. Sunita Nadella for graphing and statistical assistance, and two US EPA internal reviewers for constructive comments. The views expressed in the present study are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency.

Funding Information:
We are grateful to Rio Tinto for critical seed funding for this work. Additional funding was provided by Ecotox, a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant (RGPIN-2017-03843) to CMW, by an EPRI contract (10009699) to CMW, and a National Science Foundation grant (IOS-1754550) to MDM. MG is a Maytag Professor of Ichthyology. We thank John Goodrich-Mahoney and Jeff Thomas of EPRI for valuable advice and co-ordination, Dr. Russ Erickson of US EPA for important input, Dr. Markus Hecker of the University of Saskatchewan for fathead minnow supply, Dr. Sunita Nadella for graphing and statistical assistance, and two US EPA internal reviewers for constructive comments. The views expressed in the present study are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency.

Publisher Copyright:
© 2020 Elsevier B.V.

Keywords

Conductivity
Goldman-Hodgkin-Katz equation
Ictalurus punctatus
Lepomis macrochirus
Multi-ion toxicity (MIT) model
Pimephales promelas

Access

10.1016/j.aquatox.2020.105568

OpenUrl availability

Full text

Cite this

@article{ce8b901b1c724bf584ed324252eefbac,

title = "The potential for salt toxicity: Can the trans-epithelial potential (TEP) across the gills serve as a metric for major ion toxicity in fish?",

abstract = "An emerging Multi-Ion Toxicity (MIT) model for assessment of environmental salt pollution is based on the premise that major ion toxicity to aquatic organisms is related to a critical disturbance of the trans-epithelial potential across the gills (ΔTEP), which can be predicted by electrochemical theory. However, the model has never been evaluated physiologically. We directly tested key assumptions by examining the individual effects of eight different salts (NaCl, Na2SO4, MgCl2, MgSO4, KCl, K2SO4, CaCl2, and CaSO4) on measured TEP in three different fish species (fathead minnow, Pimephales promelas = FHM; channel catfish, Ictalurus punctatus = CC; bluegill, Lepomis macrochirus = BG). A geometric concentration series based on previously reported 96-h LC50 values for FHM was used. All salts caused concentration-dependent increases in TEP to less negative/more positive values in a pattern well-described by the Michaelis-Menten equation. The ΔTEP responses for different salts were similar to one another within each species when concentrations were expressed as a percentage of the FHM LC50. A plateau was reached at or before 100 % of the LC50 where the ΔTEP values were remarkably consistent, with only 1.4 to 2.2-fold variation. This relative uniformity in the ΔTEP responses contrasts with 28-fold variation in salt concentration (in mmol L−1), 9.6-fold in total dissolved solids, and 7.9-fold in conductivity at the LC50. The Michaelis-Menten Km values (salt concentrations causing 50 % of the ΔTEPmax) were positively related to the 96-h LC50 values. ΔTEP responses were not a direct effect of osmolarity in all species and were related to specific cation rather than specific anion concentrations in FHM. These responses were stable for up to 24 h in CC. The results provide strong physiological support for the assumptions of the MIT model, are coherent with electrochemical theory, and point to areas for future research.",

keywords = "Conductivity, Goldman-Hodgkin-Katz equation, Ictalurus punctatus, Lepomis macrochirus, Multi-ion toxicity (MIT) model, Pimephales promelas",

author = "Wood, {Chris M.} and McDonald, {M. Danielle} and Martin Grosell and Mount, {David R.} and Adams, {William J.} and Po, {Beverly H.K.} and Brix, {Kevin V.}",

note = "Funding Information: We are grateful to Rio Tinto for critical seed funding for this work. Additional funding was provided by Ecotox, a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant ( RGPIN-2017-03843 ) to CMW, by an EPRI contract ( 10009699 ) to CMW, and a National Science Foundation grant ( IOS-1754550 ) to MDM. MG is a Maytag Professor of Ichthyology. We thank John Goodrich-Mahoney and Jeff Thomas of EPRI for valuable advice and co-ordination, Dr. Russ Erickson of US EPA for important input, Dr. Markus Hecker of the University of Saskatchewan for fathead minnow supply, Dr. Sunita Nadella for graphing and statistical assistance, and two US EPA internal reviewers for constructive comments. The views expressed in the present study are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency. Funding Information: We are grateful to Rio Tinto for critical seed funding for this work. Additional funding was provided by Ecotox, a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant (RGPIN-2017-03843) to CMW, by an EPRI contract (10009699) to CMW, and a National Science Foundation grant (IOS-1754550) to MDM. MG is a Maytag Professor of Ichthyology. We thank John Goodrich-Mahoney and Jeff Thomas of EPRI for valuable advice and co-ordination, Dr. Russ Erickson of US EPA for important input, Dr. Markus Hecker of the University of Saskatchewan for fathead minnow supply, Dr. Sunita Nadella for graphing and statistical assistance, and two US EPA internal reviewers for constructive comments. The views expressed in the present study are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency. Publisher Copyright: {\textcopyright} 2020 Elsevier B.V.",

year = "2020",

month = sep,

doi = "10.1016/j.aquatox.2020.105568",

language = "English (US)",

volume = "226",

journal = "Aquatic Toxicology",

issn = "0166-445X",

publisher = "Elsevier",

}

TY - JOUR

T1 - The potential for salt toxicity

T2 - Can the trans-epithelial potential (TEP) across the gills serve as a metric for major ion toxicity in fish?

AU - Wood, Chris M.

AU - McDonald, M. Danielle

AU - Grosell, Martin

AU - Mount, David R.

AU - Adams, William J.

AU - Po, Beverly H.K.

AU - Brix, Kevin V.

N1 - Funding Information: We are grateful to Rio Tinto for critical seed funding for this work. Additional funding was provided by Ecotox, a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant ( RGPIN-2017-03843 ) to CMW, by an EPRI contract ( 10009699 ) to CMW, and a National Science Foundation grant ( IOS-1754550 ) to MDM. MG is a Maytag Professor of Ichthyology. We thank John Goodrich-Mahoney and Jeff Thomas of EPRI for valuable advice and co-ordination, Dr. Russ Erickson of US EPA for important input, Dr. Markus Hecker of the University of Saskatchewan for fathead minnow supply, Dr. Sunita Nadella for graphing and statistical assistance, and two US EPA internal reviewers for constructive comments. The views expressed in the present study are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency. Funding Information: We are grateful to Rio Tinto for critical seed funding for this work. Additional funding was provided by Ecotox, a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant (RGPIN-2017-03843) to CMW, by an EPRI contract (10009699) to CMW, and a National Science Foundation grant (IOS-1754550) to MDM. MG is a Maytag Professor of Ichthyology. We thank John Goodrich-Mahoney and Jeff Thomas of EPRI for valuable advice and co-ordination, Dr. Russ Erickson of US EPA for important input, Dr. Markus Hecker of the University of Saskatchewan for fathead minnow supply, Dr. Sunita Nadella for graphing and statistical assistance, and two US EPA internal reviewers for constructive comments. The views expressed in the present study are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency. Publisher Copyright: © 2020 Elsevier B.V.

PY - 2020/9

Y1 - 2020/9

N2 - An emerging Multi-Ion Toxicity (MIT) model for assessment of environmental salt pollution is based on the premise that major ion toxicity to aquatic organisms is related to a critical disturbance of the trans-epithelial potential across the gills (ΔTEP), which can be predicted by electrochemical theory. However, the model has never been evaluated physiologically. We directly tested key assumptions by examining the individual effects of eight different salts (NaCl, Na2SO4, MgCl2, MgSO4, KCl, K2SO4, CaCl2, and CaSO4) on measured TEP in three different fish species (fathead minnow, Pimephales promelas = FHM; channel catfish, Ictalurus punctatus = CC; bluegill, Lepomis macrochirus = BG). A geometric concentration series based on previously reported 96-h LC50 values for FHM was used. All salts caused concentration-dependent increases in TEP to less negative/more positive values in a pattern well-described by the Michaelis-Menten equation. The ΔTEP responses for different salts were similar to one another within each species when concentrations were expressed as a percentage of the FHM LC50. A plateau was reached at or before 100 % of the LC50 where the ΔTEP values were remarkably consistent, with only 1.4 to 2.2-fold variation. This relative uniformity in the ΔTEP responses contrasts with 28-fold variation in salt concentration (in mmol L−1), 9.6-fold in total dissolved solids, and 7.9-fold in conductivity at the LC50. The Michaelis-Menten Km values (salt concentrations causing 50 % of the ΔTEPmax) were positively related to the 96-h LC50 values. ΔTEP responses were not a direct effect of osmolarity in all species and were related to specific cation rather than specific anion concentrations in FHM. These responses were stable for up to 24 h in CC. The results provide strong physiological support for the assumptions of the MIT model, are coherent with electrochemical theory, and point to areas for future research.

AB - An emerging Multi-Ion Toxicity (MIT) model for assessment of environmental salt pollution is based on the premise that major ion toxicity to aquatic organisms is related to a critical disturbance of the trans-epithelial potential across the gills (ΔTEP), which can be predicted by electrochemical theory. However, the model has never been evaluated physiologically. We directly tested key assumptions by examining the individual effects of eight different salts (NaCl, Na2SO4, MgCl2, MgSO4, KCl, K2SO4, CaCl2, and CaSO4) on measured TEP in three different fish species (fathead minnow, Pimephales promelas = FHM; channel catfish, Ictalurus punctatus = CC; bluegill, Lepomis macrochirus = BG). A geometric concentration series based on previously reported 96-h LC50 values for FHM was used. All salts caused concentration-dependent increases in TEP to less negative/more positive values in a pattern well-described by the Michaelis-Menten equation. The ΔTEP responses for different salts were similar to one another within each species when concentrations were expressed as a percentage of the FHM LC50. A plateau was reached at or before 100 % of the LC50 where the ΔTEP values were remarkably consistent, with only 1.4 to 2.2-fold variation. This relative uniformity in the ΔTEP responses contrasts with 28-fold variation in salt concentration (in mmol L−1), 9.6-fold in total dissolved solids, and 7.9-fold in conductivity at the LC50. The Michaelis-Menten Km values (salt concentrations causing 50 % of the ΔTEPmax) were positively related to the 96-h LC50 values. ΔTEP responses were not a direct effect of osmolarity in all species and were related to specific cation rather than specific anion concentrations in FHM. These responses were stable for up to 24 h in CC. The results provide strong physiological support for the assumptions of the MIT model, are coherent with electrochemical theory, and point to areas for future research.

KW - Conductivity

KW - Goldman-Hodgkin-Katz equation

KW - Ictalurus punctatus

KW - Lepomis macrochirus

KW - Multi-ion toxicity (MIT) model

KW - Pimephales promelas

UR - http://www.scopus.com/inward/record.url?scp=85089246481&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85089246481&partnerID=8YFLogxK

U2 - 10.1016/j.aquatox.2020.105568

DO - 10.1016/j.aquatox.2020.105568

M3 - Article

C2 - 32791376

AN - SCOPUS:85089246481

SN - 0166-445X

VL - 226

JO - Aquatic Toxicology

JF - Aquatic Toxicology

M1 - 105568

ER -

The potential for salt toxicity: Can the trans-epithelial potential (TEP) across the gills serve as a metric for major ion toxicity in fish?

Abstract

Bibliographical note

Keywords

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this