Paralysis and heart failure precede ion balance disruption in heat-stressed European green crabs

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Paralysis and heart failure precede ion balance disruption in heat-stressed European green crabs. / Jorgensen, Lisa B.; Overgaard, Johannes; MacMillan, Heath A.

In: Journal of Thermal Biology, Vol. 68, No. Part B, 08.2017, p. 186-194.

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Jorgensen, Lisa B. ; Overgaard, Johannes ; MacMillan, Heath A. / Paralysis and heart failure precede ion balance disruption in heat-stressed European green crabs. In: Journal of Thermal Biology. 2017 ; Vol. 68, No. Part B. pp. 186-194.

Bibtex

@article{e422ae40047a45ac92a1247655308860,
title = "Paralysis and heart failure precede ion balance disruption in heat-stressed European green crabs",
abstract = "Acute exposure of ectotherms to critically high temperatures causes injury and death, and this mortality has been associated with a number of physiological perturbations including impaired oxygen transport, loss of ion and water homeostasis, and neuronal failure. It is difficult to discern which of these factors, if any, is the proximate cause of heat injury because, for example, loss of ion homeostasis can impair neuromuscular function (including cardiac function), and conversely impaired oxygen transport reduces ATP supply and can thus reduce ion transport capacity. In this study we investigated if heat stress causes a loss of ion homeostasis in marine crabs and examined if such loss is related to heart failure. We held crabs (Carcinus maenas) at temperatures just below their critical thermal maximum and measured extracellular (hemolymph) and intracellular (muscle) ion concentrations over time. Analysis of Arrhenius plots for heart rates during heating ramps revealed a breakpoint temperature below which heart rate increased with temperature, and above which heart rate declined until complete cardiac failure. As hypothesised, heat stress reduced the Nernst equilibrium potentials of both and Nat, likely causing a depolarization of the membrane potential. To examine whether this loss of ion balance was likely to cause disruption of neuromuscular function, we exposed crabs to the same temperatures, but this time measured ion concentrations at the individual-specific times of complete paralysis (from which the crabs never recovered), and at the time of cardiac failure. Loss of ion balance was observed only after both paralysis and complete heart failure had occurred; indicating that the loss of neuromuscular function is not caused by a loss of ion homeostasis. Instead we suggest that the observed loss of ion balance may be linked to tissue damage related to heat death.",
keywords = "Ion balance, Sodium, Potassium, Heat stress, Crustacean, TEMPERATURE-DEPENDENT BIOGEOGRAPHY, LIMIT THERMAL TOLERANCE, CLIMATE-CHANGE, CARCINUS-MAENAS, GENUS PETROLISTHES, OXYGEN LIMITATION, VERTICAL ZONATION, PORCELAIN CRABS, ACCLIMATION, ADAPTATION",
author = "Jorgensen, {Lisa B.} and Johannes Overgaard and MacMillan, {Heath A.}",
year = "2017",
month = "8",
doi = "10.1016/j.jtherbio.2016.08.001",
language = "English",
volume = "68",
pages = "186--194",
journal = "Journal of Thermal Biology",
issn = "0306-4565",
publisher = "Pergamon Press",
number = "Part B",

}

RIS

TY - JOUR

T1 - Paralysis and heart failure precede ion balance disruption in heat-stressed European green crabs

AU - Jorgensen, Lisa B.

AU - Overgaard, Johannes

AU - MacMillan, Heath A.

PY - 2017/8

Y1 - 2017/8

N2 - Acute exposure of ectotherms to critically high temperatures causes injury and death, and this mortality has been associated with a number of physiological perturbations including impaired oxygen transport, loss of ion and water homeostasis, and neuronal failure. It is difficult to discern which of these factors, if any, is the proximate cause of heat injury because, for example, loss of ion homeostasis can impair neuromuscular function (including cardiac function), and conversely impaired oxygen transport reduces ATP supply and can thus reduce ion transport capacity. In this study we investigated if heat stress causes a loss of ion homeostasis in marine crabs and examined if such loss is related to heart failure. We held crabs (Carcinus maenas) at temperatures just below their critical thermal maximum and measured extracellular (hemolymph) and intracellular (muscle) ion concentrations over time. Analysis of Arrhenius plots for heart rates during heating ramps revealed a breakpoint temperature below which heart rate increased with temperature, and above which heart rate declined until complete cardiac failure. As hypothesised, heat stress reduced the Nernst equilibrium potentials of both and Nat, likely causing a depolarization of the membrane potential. To examine whether this loss of ion balance was likely to cause disruption of neuromuscular function, we exposed crabs to the same temperatures, but this time measured ion concentrations at the individual-specific times of complete paralysis (from which the crabs never recovered), and at the time of cardiac failure. Loss of ion balance was observed only after both paralysis and complete heart failure had occurred; indicating that the loss of neuromuscular function is not caused by a loss of ion homeostasis. Instead we suggest that the observed loss of ion balance may be linked to tissue damage related to heat death.

AB - Acute exposure of ectotherms to critically high temperatures causes injury and death, and this mortality has been associated with a number of physiological perturbations including impaired oxygen transport, loss of ion and water homeostasis, and neuronal failure. It is difficult to discern which of these factors, if any, is the proximate cause of heat injury because, for example, loss of ion homeostasis can impair neuromuscular function (including cardiac function), and conversely impaired oxygen transport reduces ATP supply and can thus reduce ion transport capacity. In this study we investigated if heat stress causes a loss of ion homeostasis in marine crabs and examined if such loss is related to heart failure. We held crabs (Carcinus maenas) at temperatures just below their critical thermal maximum and measured extracellular (hemolymph) and intracellular (muscle) ion concentrations over time. Analysis of Arrhenius plots for heart rates during heating ramps revealed a breakpoint temperature below which heart rate increased with temperature, and above which heart rate declined until complete cardiac failure. As hypothesised, heat stress reduced the Nernst equilibrium potentials of both and Nat, likely causing a depolarization of the membrane potential. To examine whether this loss of ion balance was likely to cause disruption of neuromuscular function, we exposed crabs to the same temperatures, but this time measured ion concentrations at the individual-specific times of complete paralysis (from which the crabs never recovered), and at the time of cardiac failure. Loss of ion balance was observed only after both paralysis and complete heart failure had occurred; indicating that the loss of neuromuscular function is not caused by a loss of ion homeostasis. Instead we suggest that the observed loss of ion balance may be linked to tissue damage related to heat death.

KW - Ion balance

KW - Sodium

KW - Potassium

KW - Heat stress

KW - Crustacean

KW - TEMPERATURE-DEPENDENT BIOGEOGRAPHY

KW - LIMIT THERMAL TOLERANCE

KW - CLIMATE-CHANGE

KW - CARCINUS-MAENAS

KW - GENUS PETROLISTHES

KW - OXYGEN LIMITATION

KW - VERTICAL ZONATION

KW - PORCELAIN CRABS

KW - ACCLIMATION

KW - ADAPTATION

U2 - 10.1016/j.jtherbio.2016.08.001

DO - 10.1016/j.jtherbio.2016.08.001

M3 - Journal article

VL - 68

SP - 186

EP - 194

JO - Journal of Thermal Biology

JF - Journal of Thermal Biology

SN - 0306-4565

IS - Part B

ER -