Acid–base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost

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 HCO(3)(-) 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% CO(2)). Fish exhibited a well-developed ability to increase plasma HCO(3)(-) levels with values of 39.8 ± 2.8 mmol l(-1) being achieved at the most severe stage of hypercapnic exposure (arterial blood PCO(2) = 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 HCO(3)(-) during hypercapnia was associated with marked increases in branchial net acid excretion (J (NET)H(+)) owing exclusively to increases in the titratable alkalinity component; total ammonia excretion was actually reduced during hypercapnia. The increase in J (NET)H(+) 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 HCO(3)(-) concentrations of 92.2 ± 4.8 mmol l(-1). At the highest level of hypercapnia, rectal fluid HCO(3)(-) 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 HCO(3)(-) to compensate for hypercapnic acidosis occurred against a backdrop of increasing intestinal HCO(3)(-) 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 HCO(3)(-) 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 HCO(3)(-). The apparent inability of P. notatus to effectively excrete HCO(3)(-) following hypercapnia may reflect its aglomerular (i.e., non-filtering) kidney coupled with the normally low rates of urine production in marine teleosts.

Ocean Acidification Leads to Counterproductive Intestinal Base Loss in the Gulf Toadfish (Opsanus beta)

“…Ϫ HCO 3 Rectal base excretion rates have been previously estimated to be as high as 135 mmol kg Ϫ1 h Ϫ1 in fish exposed to 5% CO 2 (Perry et al 2010). Together these studies support a dosedependent, although not linear, response.…”

Juvenile Antarctic rockcod,Trematomus bernacchii, are physiologically robust to CO2–acidified seawater

“…The respiratory physiology of fishes does facilitate excretion of CO 2 from the countercurrent exchange from water to blood and unidirectional water flow across the gills to maintain stable blood pH (Heuer and Grosell, 2014). However, more common mechanisms for acid-base balance in fish include the secretion of H + and the retention and absorption of HCO 3 − through different ion exchanges and de novo synthesis of HCO 3 − by the kidney (Wright, 1995;Wood et al, 1999;Lawrence et al, 2015), facilitated by carbonic anhydrase Perry et al, 2010;Esbaugh et al, 2012;Tseng et al, 2013). Future studies could quantify plasma HCO 3…”

“…and P CO2 and analyze the activity or mRNA expression of these enzymes and transporters to provide additional insight into any acid-base imbalances that might have occurred in response to elevated P CO2 (Melzner et al, 2009;Perry et al, 2010;Esbaugh et al, 2012;Lawrence et al, 2015).…”

Factors influencing cannibalism in the plainfin midshipman fish

“…As the tides retreat, these guarder males do not leave their nests, even as the small pools of remaining water become hypoxic (Craig et al, 2014). Males can endure these hypoxic conditions through metabolic suppression, a switch to anaerobic pathways (Craig et al, 2014) and a welladapted system for acidebase regulation (Perry et al, 2010). The guarder males produce an acoustic signal with a specially adapted swim bladder encased in a sonic muscle capable of generating longduration, low-frequency vibrations (Bass & Marchaterre, 1989;Sisneros & Bass, 2003) to attract gravid females to their nests (Brantley & Bass, 1994;Brantley et al, 1993;Ibara, Penny, Ebeling, van Dykhuizen, & Cailliet, 1983).…”