Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alterations in a coral reef fish

Abstract

Neurosensory and behavioural disruptions are some of the most consistently reported responses upon exposure to ocean acidification-relevant CO2 levels, especially in coral reef fishes. The underlying cause of these disruptions is thought to be altered current across the GABAA receptor in neuronal cells due to changes in ion gradients (HCO3− and/or Cl−) that occur in the body following compensation for elevated ambient CO2. Despite these widely-documented behavioural disruptions, the present study is the first to pair a behavioural assay with measurements of relevant intracellular and extracellular acid-base parameters in a coral reef fish exposed to elevated CO2. Spiny damselfish (Acanthochromis polyacanthus) exposed to 1900 μatm CO2 for 4 days exhibited significantly increased intracellular and extracellular HCO3− concentrations and elevated brain pHi compared to control fish, providing evidence of CO2 compensation. As expected, high CO2 exposed damselfish spent significantly more time in a chemical alarm cue (CAC) than control fish, supporting a potential link between behavioural disruption and CO2 compensation. Using HCO3− measurements from the damselfish, the reversal potential for GABAA (EGABA) was calculated, illustrating that biophysical properties of the brain during CO2 compensation could change GABAA receptor function and account for the behavioural disturbances noted during exposure to elevated CO2.

Expression of genes involved in brain GABAergic neurotransmission in three-spined stickleback exposed to near-future CO2

“…Exposure to high CO 2 levels triggers acid–base adjustments in fish involving altered levels of Cl − and HCO 3 − (Brauner and Baker, 2009), which have been suggested to change neuronal membrane gradients of these ions, switching some GABA A receptors from being inhibitory to excitatory (Nilsson et al ., 2012). Based on the scarce data available, calculations of GABA A equilibrium potentials of neurons in fish exposed to near-future pCO 2 are consistent in showing a possibility for a shift in the GABA A receptor equilibrium potential from causing hyperpolarization to depolarization (Heuer and Grosell, 2014; Nilsson and Lefevre, 2016; Heuer et al ., 2016; Regan et al ., 2016). Here, we hypothesized that an increase in CO 2 levels in the marine environment, triggering acid–base regulatory mechanisms in fish, could lead to changes in the expression of genes involved in regulating GABA A receptor function and neuronal ion distribution.…”

“…Heuer et al . (2016) showed that the increase in plasma partial pressure of CO 2 (in millimetres of mercury) in spiny damselfish ( Acanthochormis polyacanthus ) kept in high-CO 2 conditions was accompanied by increases in intracellular and extracellular HCO 3 − concentrations, with an assumed decrease in intracellular Cl − (Heuer et al ., 2016). Based on their measurements, they calculated a positive deviation in the E GABAA resting potential in fish exposed to 1900 µatm CO 2 , consistent with a shift in the GABA action towards depolarization (excitation) rather than hyperpolarization (inhibition).…”

Predatory strategies and behaviours in cephalopods are altered by elevated CO2

“…This complex network of millions of neurons responsible for altering body patterns in cephalopods contain “all of the ‘classic’ neurotransmitters”, including γ‐aminobutyric acid (GABA) which are distributed throughout all neural lobes controlling chromatophore function (Messenger, ). GABA‐A receptors are important in this context as they appear to be responsible for the behavioural changes in other molluscs (Watson et al., ) and fishes (Hamilton, Holcombe, & Tresguerres, ; Heuer, Welch, Rummer, Munday, & Grosell, ; Lai, Jutfelt, & Nilsson, ; Nilsson et al., ) resulting from elevated CO 2 . Recent molecular analyses also demonstrate that substantial changes to GABA pathways are a feature of high CO 2 exposure in other invertebrates (Moya et al., ) and fish (Schunter et al., ), further supporting a role in behavioural changes.…”

Acid–base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification

“…P CO2 between 600 and 2000 µatm). The pattern that emerged was complete regulation of blood plasma pH and a 2-5 mmol l −1 increase in blood plasma [HCO 3 − ] Esbaugh et al, 2016Esbaugh et al, , 2012Green and Jutfelt, 2014;Heinrich et al, 2014;Heuer et al, 2016;Strobel et al, 2012) (Table 1). Only three studies measured blood plasma [Cl − ], but none of them found significant changes after exposure to OA-like conditions Green and Jutfelt, 2014;Heinrich et al, 2014).…”

“…To our knowledge, only Heuer et al (2016) have estimated A-B parameters in the brains of fish exposed to OA-relevant P CO2 levels. and theoretical GABA A R Cl − and HCO 3 − permeability ratios, the results generally supported the GABA A R model.…”