Abstract
The plainfin midshipman (Porichthys notatus) possesses an aglomerular kidney and like other marine teleosts, secretes base into the intestine to aid water absorption. Each of these features could potentially influence acid–base regulation during respiratory acidosis either by facilitating or constraining HCO3 − accumulation, respectively. Thus, in the present study, we evaluated the capacity of P. notatus to regulate blood acid–base status during exposure to increasing levels of hypercapnia (nominally 1–5% CO2). Fish exhibited a well-developed ability to increase plasma HCO3 − levels with values of 39.8 ± 2.8 mmol l−1 being achieved at the most severe stage of hypercapnic exposure (arterial blood PCO2 = 21.9 ± 1.7 mmHg). Consequently, blood pH, while lowered by 0.15 units (pH = 7.63 ± 0.06) during the final step of hypercapnia, was regulated far above values predicted by chemical buffering (predicted pH = 7.0). The accumulation of plasma HCO3 − during hypercapnia was associated with marked increases in branchial net acid excretion (J NETH+) owing exclusively to increases in the titratable alkalinity component; total ammonia excretion was actually reduced during hypercapnia. The increase in J NETH+ was accompanied by increases in branchial carbonic anhydrase (CA) enzymatic activity (2.8×) and CA protein levels (1.6×); branchial Na+/K+-ATPase activity was unaffected. Rectal fluids sampled from control fish contained on average HCO3 − concentrations of 92.2 ± 4.8 mmol l−1. At the highest level of hypercapnia, rectal fluid HCO3 − levels were increased significantly to 141.8 ± 7.4 mmol l−1 but returned to control levels during post-hypercapnia recovery (96.0 ± 13.2 mmol l−1). Thus, the impressive accumulation of plasma HCO3 − to compensate for hypercapnic acidosis occurred against a backdrop of increasing intestinal HCO3 − excretion. Based on in vitro measurements of intestinal base secretion in Ussing chambers, it would appear that P. notatus did not respond by minimizing base loss during hypercapnia; the increases in base flux across the intestinal epithelium in response to alterations in serosal HCO3 − concentration were similar in preparations obtained from control or hypercapnic fish. Fish returned to normocapnia developed profound metabolic alkalosis owing to unusually slow clearance of the accumulated plasma HCO3 −. The apparent inability of P. notatus to effectively excrete HCO3 − following hypercapnia may reflect its aglomerular (i.e., non-filtering) kidney coupled with the normally low rates of urine production in marine teleosts.
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Acknowledgments
The costs of research were supported by Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery and Research Tools and Innovation grants to S.F.P. and K.M.G. and an NSF grant (IAB 0743903) to M.G. M.H.B., B.V. and J.T. received Journal of Experimental Biology Travelling Fellowships. We are grateful to local fish providers (Robert, Delores and James Bowker of Bamfield, BC and Raymond Martel of Parksville, BC). We are forever indebted to Dr. Bruce Cameron, BMSC Research Director, for his tireless support.
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Perry, S.F., Braun, M.H., Genz, J. et al. Acid–base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost. J Comp Physiol B 180, 1213–1225 (2010). https://doi.org/10.1007/s00360-010-0492-8
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DOI: https://doi.org/10.1007/s00360-010-0492-8