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First published online November 17, 2006
Journal of Experimental Biology 209, 4701-4716 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02564

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A critical analysis of carbonic anhydrase function, respiratory gas exchange, and the acid-base control of secretion in the rectal gland of Squalus acanthias

Trevor J. Shuttleworth^1,2, Jill Thompson^1,2, R. Stephen Munger^2,3,4 and Chris M. Wood^2,4,*

¹ Department of Pharmacology and Physiology, University of Rochester School of Medicine and Dentistry, Rochester, NY 14642, USA
² Bamfield Marine Sciences Centre, 100 Pachena Drive, Bamfield, British Columbia, VOR 1BO, Canada
³ Canadian Nuclear Safety Commission, PO Box 1046, Station B, 280 Slater Street, Ottawa, Ontario, K1P 5S9, Canada
⁴ Department of Biology, McMaster University, 1280 Main St. West, Hamilton, Ontario, L8S 4K1, Canada

View larger version (14K): [in a new window]   Fig. 1. The influence of acetazolamide (20 mg kg-1) administered at 3 h on: (A) rectal gland Cl- secretion rate: (B) arterial pH; (C) arterial CO2 tension; and (D) arterial plasma bicarbonate concentration. Values are means ± 1 s.e.m. Control data are from fish (N=7) identically infused with 500 mmol l-1 NaCl but not treated with acetazolamide. *Values significantly different (P<0.05) from the simultaneous value in the control treatment; values significantly different (P<0.05) from the pre-treatment reference values in the same treatment group.

View larger version (13K): [in a new window]   Fig. 2. (A) The relationship between secretion flow rate (x axis) and Cl- secretion rate (y axis) in perfused rectal gland preparations stimulated with 5x10-6 mol l-1 forskolin. y=0.52x-0.01 (r=0.99, N=127, P<0.0001). The slope (0.52) of the regression line indicates that the average concentration of Cl- in the secretion was 520 mmol l-1. Simultaneous measurements obtained at high perfusion pressure (20 mmHg), reduced perfusion pressure (12 mmHg), and after all experimental treatments at reduced perfusion pressure (12 mmHg), are plotted: N=127 data points from 71 preparations. (B). Open triangles: the relationship between Cl- secretion rate (x) and oxygen consumption rate (; y) in all perfused rectal gland preparations. y=0.022x+0.11 (r=0.73, N=139, P<0.0001). Simultaneous measurements obtained at high perfusion pressure (20 mmHg) in the absence of stimulation (no Cl- secretion), and in the presence of stimulation with 5.5x10-6 mol l-1 forskolin at high perfusion pressure (20 mmHg), at reduced perfusion pressure (12 mmHg), and after all experimental treatments at reduced perfusion pressure (12 mmHg), are plotted: N=139 data points from 71 preparations. Closed circles: the relationship between Cl- secretion rate (x) and carbon dioxide excretion rate (; y) in perfused rectal gland preparations. y=0.036x+0.22 (r=0.48, N=117, P<0.0001). The same set of simultaneous measurements as used for are plotted, with the exception of points obtained at high perfusate HCO3- concentration (where it was impossible to resolve small arterial-venous differences in total CO2 concentrations) and after treatment with acetazolamide (which transiently inhibited CO2 excretion). N=117 data points from 68 preparations.

View larger version (15K): [in a new window]   Fig. 3. The influence of 10-4 mol l-1 acetazolamide added to the perfusion saline at 0 h on (A) Cl- secretion rate, (B) oxygen consumption rate () and (C) carbon dioxide excretion rate () in the perfused rectal gland. Asterisks indicate means significantly different (P<0.05) from the control value at `C' before acetazolamide addition. Values are means ± 1 s.e.m. (N=6).

View larger version (7K): [in a new window]   Fig. 4. The influence of 10-4 mol l-1 acetazolamide added to the perfusion saline at 0 h on PCO2 levels in arterial perfusate inflow, venous perfusate outflow, and secretion fluid. Asterisks indicate means significantly different (P<0.05) from the respective control value at `C' before acetazolamide addition. Values are means ± 1 s.e.m. (N=6).

View larger version (18K): [in a new window]   Fig. 5. The influence of experimental manipulations of acid-base status on the relative rate of Cl- secretion rate in the perfused rectal gland. Secretion rate after 2 h of experimental treatment is expressed as a percentage of the pre-treatment control (Con) measurement. Measured values of extracellular pHe and intracellular pHi are given; for other acid-base parameters, see Table 4. Means sharing the same letter are not significantly different (P>0.05). Values are means (+1 s.e.m.) (N=6-7).

View larger version (5K): [in a new window]   Fig. 6. The relationship between extracellular pHe (x) and relative Cl- secretion rate (y) of the isolated-perfused rectal gland activated by 5x10-6 mol l-1 forskolin (closed symbols, data from Fig. 5 of the present study) and the rectal gland of intact, unanaesthetized dogfish activated by systemic volume loading [open symbols, data from Wood et al. (Wood et al., 2006)]. Data from every experimental treatment except acetazolamide are shown. Values are means ± 1 s.e.m. (N=5-7 for each treatment). The in vitro and in vivo data sets appear to follow a single relationship. The equation of the exponential regression line is: y=0.0441e0.9784x (r=0.94, P<0.0001).