Water pH limits extracellular but not intracellular pH compensation in the CO2-tolerant freshwater fish Pangasianodon hypophthalmus

ABSTRACT Preferentially regulating intracellular pH (pHi) confers exceptional CO2 tolerance on fish, but is often associated with reductions in extracellular pH (pHe) compensation. It is unknown whether these reductions are due to intrinsically lower capacities for pHe compensation, hypercarbia-induced reductions in water pH or other factors. To test how water pH affects capacities and strategies for pH compensation, we exposed the CO2-tolerant fish Pangasianodon hypophthalmus to 3 kPa PCO2 for 20 h at an ecologically relevant water pH of 4.5 or 5.8. Brain, heart and liver pHi was preferentially regulated in both treatments. However, blood pHe compensation was severely reduced at water pH 4.5 but not 5.8. This suggests that low water pH limits acute pHe but not pHi compensation in fishes preferentially regulating pHi. Hypercarbia-induced reductions in water pH might therefore underlie the unexplained reductions to pHe compensation in fishes preferentially regulating pHi, and may increase selection for preferential pHi regulation. Summary: Low water pH limits extracellular pH compensation in a CO2-tolerant fish. This may increase selection for a more robust CO2 defence strategy where intracellular pH is preferentially regulated.

[1]  2015 Lower Mekong Regional Water Quality Monitoring Report , 2018 .

[2]  C. Brauner,et al.  Effects of water ionic composition on acid–base regulation in rainbow trout, during hypercarbia at rest and during sustained exercise , 2018, Journal of Comparative Physiology B.

[3]  C. Brauner,et al.  Characterization of Na+ transport to gain insight into the mechanism of acid-base and ion regulation in white sturgeon (Acipenser transmontanus). , 2017, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[4]  D. Crossley,et al.  Preferential intracellular pH regulation: hypotheses and perspectives , 2016, Journal of Experimental Biology.

[5]  C. Damsgaard,et al.  Recovery of blood gases and haematological parameters upon anaesthesia with benzocaine, MS-222 or Aqui-S in the air-breathing catfish Pangasianodon hypophthalmus , 2016, Ichthyological Research.

[6]  C. Damsgaard,et al.  High capacity for extracellular acid–base regulation in the air-breathing fish Pangasianodon hypophthalmus , 2015, The Journal of Experimental Biology.

[7]  Rossana Occhipinti,et al.  Mathematical modeling of acid-base physiology. , 2015, Progress in biophysics and molecular biology.

[8]  C. Brauner,et al.  Acid-base and ion balance in fishes with bimodal respiration. , 2014, Journal of fish biology.

[9]  S. Perry,et al.  The physiology of fish at low pH: the zebrafish as a model system , 2014, Journal of Experimental Biology.

[10]  T. Gomi,et al.  Human factors and tidal influences on water quality of an urban river in Can Tho, a major city of the Mekong Delta, Vietnam , 2014, Environmental Monitoring and Assessment.

[11]  S. Perry,et al.  Acid–base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost , 2010, Journal of Comparative Physiology B.

[12]  G. Goss,et al.  Intracellular pH regulation in isolated trout gill mitochondrion-rich (MR) cell subtypes: evidence for Na+/H+ activity. , 2010, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[13]  D. Baker Physiological responses associated with aquatic hypercarbia in the CO₂-tolerant white sturgeon, Acipenser transmontanus , 2010 .

[14]  C. Brauner,et al.  A validation of intracellular pH measurements in fish exposed to hypercarbia: the effect of duration of tissue storage and efficacy of the metabolic inhibitor tissue homogenate method. , 2009, Journal of fish biology.

[15]  C. Brauner,et al.  Patterns of Acid–Base Regulation During Exposure to Hypercarbia in Fishes , 2009 .

[16]  V. Matey,et al.  Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. , 2009, American journal of physiology. Regulatory, integrative and comparative physiology.

[17]  R. Naiman,et al.  Freshwater biodiversity: importance, threats, status and conservation challenges , 2006, Biological reviews of the Cambridge Philosophical Society.

[18]  O. Kepp,et al.  Evolution of Oxygen Secretion in Fishes and the Emergence of a Complex Physiological System , 2005, Science.

[19]  C. Wood,et al.  Ionoregulation in Tropical Fishes from Ion‐Poor, Acidic Blackwaters , 2005 .

[20]  A. Val,et al.  Limited extracellular but complete intracellular acid-base regulation during short-term environmental hypercapnia in the armoured catfish, Liposarcus pardalis , 2004, Journal of Experimental Biology.

[21]  F. Jensen,et al.  Influence of ionic composition on acid-base regulation in rainbow trout (Oncorhynchus mykiss) exposed to environmental hypercapnia , 1997, Fish Physiology and Biochemistry.

[22]  Jun Kita,et al.  Acid-base responses to lethal aquatic hypercapnia in three marine fishes , 2004 .

[23]  J. Steffensen,et al.  Tolerance of chronic hypercapnia by the European eel Anguilla anguilla , 2003, Journal of Experimental Biology.

[24]  A. Morrison-Shetlar,et al.  Acid-base regulation in fishes: cellular and molecular mechanisms. , 2002, The Journal of experimental zoology.

[25]  W. Junk,et al.  Physicochemical Conditions in the Floodplains , 1997 .

[26]  D. Randall,et al.  9 Proton Pumps in Fish Gills , 1995 .

[27]  C. Wood,et al.  Intracellular acid-base responses to environmental hyperoxia and normoxic recovery in rainbow trout. , 1991, Respiration physiology.

[28]  H. Pörtner,et al.  Determination of intracellular pH and PCO2 after metabolic inhibition by fluoride and nitrilotriacetic acid. , 1990, Respiration physiology.

[29]  K. Groebe,et al.  Role of geometry and anisotropic diffusion for modelling PO2 profiles in working red muscle. , 1990, Respiration physiology.

[30]  D. Mcdonald,et al.  Physiological correlates of interspecific variation in acid tolerance in fish , 1988 .

[31]  G. R. Ultsch Blood Gases, Hematocrit, Plasma Ion Concentrations, and Acid-Base Status of Musk Turtles (Sternotherus odoratus) during Simulated Hibernation , 1988, Physiological Zoology.

[32]  K. Dimberg High blood CO2 levels in rainbow trout exposed to hypercapnia in bicarbonate-rich hard fresh water--a methodological verification. , 1988, The Journal of experimental biology.

[33]  N. Heisler 6 Acid-Base Regulation in Fishes* , 1984 .

[34]  R. Boutilier,et al.  Appendix: Physicochemical Parameters for use in Fish Respiratory Physiology* , 1984 .

[35]  N. Heisler Intracellular and extracellular acid-base regulation in the tropical fresh-water teleost fish Synbranchus marmoratus in response to the transition from water breathing to air breathing. , 1982, The Journal of experimental biology.

[36]  P. Stewart,et al.  Independent and dependent variables of acid-base control. , 1978, Respiration physiology.

[37]  R. Zeidler,et al.  Preferential hemolysis of postnatal calf red cells induced by internal alkanlinization , 1977, The Journal of general physiology.