Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels

Regan, Matthew D.; Turko, Andy J.; Heras, Joseph; Andersen, Mads Kuhlmann; Lefevre, Sjannie; Wang, Tobias; Bayley, Mark; Brauner, Colin J.; Hương, Đỗ Thị Thanh; Phương, Nguyễn Thanh; Nilsson, Göran

doi:10.1242/jeb.131375

Cited by 55 publications

(29 citation statements)

References 54 publications

(77 reference statements)

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“…The GABA A R model does seem to fit with principles of basic neuroscience, but it must be validated with more than the use of gabazine and behavioural studies. Nilsson and Lefevre, 2016;Regan et al, 2016). However, only a few studies have measured these parameters in the blood plasma of fish exposed to OA-relevant conditions (i.e.…”

Section: Pharmacological Considerationsmentioning

confidence: 99%

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

Tresguerres

Hamilton

2017

Journal of Experimental Biology

103

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Experimental exposure to ocean and freshwater acidification affects the behaviour of multiple aquatic organisms in laboratory tests. One proposed cause involves an imbalance in plasma chloride and bicarbonate ion concentrations as a result of acid-base regulation, causing the reversal of ionic fluxes through GABA A receptors, which leads to altered neuronal function. This model is exclusively based on differential effects of the GABA A receptor antagonist gabazine on control animals and those exposed to elevated CO 2 . However, direct measurements of actual chloride and bicarbonate concentrations in neurons and their extracellular fluids and of GABA A receptor properties in aquatic organisms are largely lacking. Similarly, very little is known about potential compensatory mechanisms, and about alternative mechanisms that might lead to ocean acidificationinduced behavioural changes. This article reviews the current knowledge on acid-base physiology, neurobiology, pharmacology and behaviour in relation to marine CO 2 -induced acidification, and identifies important topics for future research that will help us to understand the potential effects of predicted levels of aquatic acidification on organisms.

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Section: Pharmacological Considerationsmentioning

confidence: 99%

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

Tresguerres

Hamilton

2017

Journal of Experimental Biology

103

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“…Tissues (heart, brain, liver, white muscle, kidney and lung) were quickly dissected (within 5 min), placed in micro-centrifuge tubes, frozen in liquid nitrogen and stored at −80°C for later measurements of pH i . Tissue was subsequently ground under liquid nitrogen and pH i was measured using the metabolic inhibitor tissue homogenate method; this technique has been validated (Baker et al, 2009b;Portner et al, 1990) and used in fish (Baker and Brauner, 2012;Baker et al, 2015;Brauner et al, 2004;Regan et al, 2016) and non-fish (Busk et al, 1997;Galli and Richards, 2012) studies. Plasma Na + , K + , Cl − and Ca 2+ were measured in embryos at 90% of incubation at each rearing condition using Stat Profile Prime (Nova Biomedical, Waltham, MA, USA).…”

Section: Blood Sampling Tissue Sampling and Ions Embryosmentioning

confidence: 99%

Embryonic common snapping turtles (Chelydra serpentina) preferentially regulate intracellular tissue pH during acid-base challenges

Shartau

Crossley

Kohl

et al. 2016

Journal of Experimental Biology

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The nests of embryonic turtles naturally experience elevated CO 2 (hypercarbia), which leads to increased blood P CO2 and a respiratory acidosis, resulting in reduced blood pH [extracellular pH ( pH e )]. Some fishes preferentially regulate tissue pH [intracellular pH ( pH i )] against changes in pH e ; this has been proposed to be associated with exceptional CO 2 tolerance and has never been identified in amniotes. As embryonic turtles may be CO 2 tolerant based on nesting strategy, we hypothesized that they preferentially regulate pH i , conferring tolerance to severe acute acid-base challenges. This hypothesis was tested by investigating pH regulation in common snapping turtles (Chelydra serpentina) reared in normoxia then exposed to hypercarbia (13 kPa P CO2 ) for 1 h at three developmental ages: 70% and 90% of incubation, and yearlings. Hypercarbia reduced pH e but not pH i , at all developmental ages. At 70% of incubation, pH e was depressed by 0.324 pH units while pH i of brain, white muscle and lung increased; heart, liver and kidney pH i remained unchanged. At 90% of incubation, pH e was depressed by 0.352 pH units but heart pH i increased with no change in pH i of other tissues. Yearlings exhibited a pH e reduction of 0.235 pH units but had no changes in pH i of any tissues. The results indicate common snapping turtles preferentially regulate pH i during development, but the degree of response is reduced throughout development. This is the first time preferential pH i regulation has been identified in an amniote. These findings may provide insight into the evolution of acid-base homeostasis during development of amniotes, and vertebrates in general.

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“…Recent studies have shown that ecologically important behavioral traits, such as activity and boldness, are affected by various emerging aquatic contaminants (Reyhanian et al, 2011;Brodin et al, 2013;Dzieweczynski et al, 2016) as well as other contaminants including inorganic mercury (Pereira et al, 2016), persistent organic pollutants (Vignet et al, 2015), and mining waste leachate (Lanctôt et al, 2016). Effects on boldness and activity have also been noted in response to ongoing large-scale changes in carbon dioxide (CO 2 ) concentrations in oceans and freshwaters (Munday et al, 2009(Munday et al, , 2010Welch et al, 2014;Regan et al, 2016). In other words, many laboratory assays imply that fish may change their activity and boldness in response to various environmental changes.…”

Section: Introductionmentioning

confidence: 99%

Drug-Induced Behavioral Changes: Using Laboratory Observations to Predict Field Observations

Klaminder

Hellström

Fahlman

et al. 2016

Front. Environ. Sci.

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Behavioral assays constitute important research tools when assessing how fish respond to environmental change. However, it is unclear how behavioral modifications recorded in laboratory assays are expressed in natural ecosystems, a limitation that makes it difficult to evaluate the predictive power of laboratory-based measurements. In this study, we hypothesized that exposure to a benzodiazepine (i.e., oxazepam) increases boldness and activity in laboratory assays as well as in field assays-that is, laboratory results can be used to predict field results. Moreover, we expected the modified behavior to affect other important ecological measures such as habitat selection and home range. To test our hypothesis, we exposed European perch (Perca fluviatilis) to oxazepam and measured subsequent changes in behavioral trials both in laboratory assays and in a lake ecosystem populated with a predatory fish species, pike (Esox lucius). In the lake, the positions of both perch and pike were tracked every 3 min for a month using acoustic telemetry. In the laboratory assay, the oxazepam-exposed perch were bolder and more active than the non-exposed perch. In the lake assay, the oxazepam-exposed perch were also more bold and active, had a larger home range, and used pelagic habitats more than the non-exposed perch. We conclude that ecotoxicological behavioral assays are useful for predicting the effects of exposure in natural systems. However, although individual responses to exposure were similar in both the laboratory and field trials, effects were more obvious in the field study, mainly due to reduced variability in the behavioral measures from the lake. Hence, short-term behavioral assays may fail to detect all the effects expressed in natural environments. Nevertheless, our study clearly demonstrates that behavioral modifications observed in laboratory settings can be used to predict how fish perform in aquatic ecosystems.

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Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels

Cited by 55 publications

References 54 publications

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

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

Embryonic common snapping turtles (Chelydra serpentina) preferentially regulate intracellular tissue pH during acid-base challenges

Drug-Induced Behavioral Changes: Using Laboratory Observations to Predict Field Observations

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