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First published online March 14, 2005
Journal of Experimental Biology 208, 1095-1107 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01480

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Cardiorespiratory responses to hypercarbia in tambaqui Colossoma macropomum: chemoreceptor orientation and specificity

K. M. Gilmour^1,2,*, W. K. Milsom^1,3, F. T. Rantin¹, S. G. Reid^1,4 and S. F. Perry^1,2

¹ Department of Physiological Sciences, Federal University of São Carlos, Via Washington Luiz km 235, São Carlos, SP, 13565-905, Brazil
² Department of Biology, University of Ottawa, 150 Louis Pasteur, Ottawa, ON, K1N 6N5 Canada
³ Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4 Canada
⁴ Department of Life Sciences, University of Toronto at Scarborough, Toronto, ON, M1C 1A4 Canada

View larger version (31K): [in a new window]   Fig. 1. The effects of stepwise increases in water PCO2 (PwCO2) followed by the rapid lowering of PwCO2 (A) on ventilation, blood gases, and acid-base status in tambaqui Colossoma macropomum, including (B) ventilation amplitude (VAMP; N=9-11), (C) ventilation frequency (fV; N=8-9), (D) arterial PCO2 (PaCO2; N=8-9), (E) arterial PO2 (PaO2; N=7-8) and (F) arterial pH (pHa; N=8-9). Pre1 and Pre2 refer to pre-exposure values compiled 2 min and immediately, respectively, before the onset of hypercarbia; the numbers 7, 16 and 26 denote values compiled for the final 2 min of the three discrete steps of increasing hypercarbia; and the data plotted to the right of the break in the x-axis represent values compiled for 2 min intervals after the initiation of rapid washout of CO2 at 0 min. The data are presented as means ± 1 S.E.M. For stepwise increases in PwCO2, values that do not share a letter are significantly different from one another (one-way RM-ANOVA, P<0.001 for B-D and F; P=0.001 for E). For the rapid washout of water CO2, asterisks indicate values that are significantly different from the value at time=0 min (one-way RM-ANOVA, P<0.001 for all).

View larger version (34K): [in a new window]   Fig. 2. The effects of stepwise increases in water PCO2 (PwCO2) followed by the rapid lowering of PwCO2 (A) on cardiovascular variables in tambaqui Colossoma macropomum including (B) arterial blood pressure (PDA; N=10-11), (C) systemic vascular resistance (Rs; N=9-10), (D) cardiac output (b; N=8-10), (E) heart rate (fH; N=9-11) and (F) cardiac stroke volume (VS; N=9-10). Data for PaCO2 are replotted from Fig. 1 in A for ease of comparison. Pre1 and Pre2 refer to pre-exposure values compiled 2 min and immediately, respectively, before the onset of hypercarbia; the numbers 7, 16 and 26 denote values compiled for the final 2 min of the three discrete steps of increasing hypercarbia; and the data plotted to the right of the break in the x-axis represent values compiled for 2 min intervals after the initiation of rapid washout of CO2 at 0 min. The data are presented as means ± 1 S.E.M. For stepwise increases in PwCO2, values that do not share a letter are significantly different from one another (one-way RM-ANOVA; P values: B, 0.386; C, 0.892; D, 0.144; E and F, <0.001). For the rapid washout of water CO2, asterisks indicate values that are significantly different from the value at time=0 min (one-way RM-ANOVA, P values: B, 0.444; C, 0.002; D-F, <0.001).

View larger version (28K): [in a new window]   Fig. 3. The effects of acetazolamide (Az) injection followed by hypercarbia (PwCO2=13.6 mmHg) and the rapid lowering of PwCO2 (A) on ventilation and blood gas and acid-base status in tambaqui Colossoma macropomum, including (B) ventilation amplitude (VAMP; N=8), (C) ventilation frequency (fV; N=8), (D) arterial PCO2 (PaCO2; N=8), (E) arterial PO2 (PaO2; N=6-7), and (F) arterial pH (pHa; N=8). Acetazolamide was injected at time=0 min, while the onset of hypercarbia and rapid water CO2 washout are designated by the vertical broken lines. Values are means ± 1 S.E.M. Significant differences from the pre-injection (time=0 min) or pre-hypercarbic exposure (time= 35 min) values are indicated by an asterisk (one-way RM-ANOVA; P values for acetazolamide treatment and hypercarbia, respectively: B, 0.127 and 0.002; C, 0.569 and <0.001; D, <0.001 for both; E, 0.241 and 0.028; F, <0.001 for both). For the rapid lowering of PwCO2, significant differences from the initial value (time=50 min) are indicated by an asterisk or double-arrowhead line (one-way RM-ANOVA with P values <0.001 for all).

View larger version (32K): [in a new window]   Fig. 4. The effects of acetazolamide (Az) injection followed by hypercarbia (PwCO2=13.6 mmHg) and the rapid lowering of PwCO2 (A) on cardiovascular variables in tambaqui Colossoma macropomum, including (B) arterial blood pressure (PDA; N=7-8), (C) systemic vascular resistance (Rs; N=6-7), (D) cardiac output (b; N=7), (E) heart rate (fH; N=8), and (F) cardiac stroke volume (VS; N=7). Data for PaCO2 are replotted from Fig. 3 in A for ease of comparison. Acetazolamide was injected at time=0 min, while the onset of hypercarbia and rapid water CO2 washout are designated by the vertical broken lines. Values are means ± 1 S.E.M. Significant differences from the pre-injection (time= 0 min) or pre-hypercarbic exposure (time=35 min) values are indicated by an asterisk (one-way RM-ANOVA; P values for acetazolamide treatment and hypercarbia, respectively: B, 0.248 and 0.045; C, 0.050 and 0.116; D, 0.016 and 0.134; E, 0.291 and 0.012; F, 0.038 and 0.006). For the rapid lowering of PwCO2, significant differences from the initial value (time= 50 min) are indicated by an asterisk or double-arrowhead line (one-way RM-ANOVA with P values: B, 0.281; C, 0.107; D, 0.011; E, 0.042; F, 0.017).

View larger version (33K): [in a new window]   Fig. 5. Representative data acquisition traces illustrating the lack of correspondence between changes in arterial PCO2 (PaCO2; red trace, A), and those in ventilation, presented as the raw impedance trace (grey, B) overlain by the calculated ventilation amplitude (VAMP) trace (black line, B). Rather, as the yellow area emphasizes, ventilation tracked changes in water PCO2 (PwCO2; black line, B).

View larger version (31K): [in a new window]   Fig. 6. (A-C,E-G) The effects of external injections of CO2-enriched water (black circles) or CO2-free acidified water (white circles) on heart rate (fH; A-C; N=16-17 for CO2-enriched water and N=7 for acidified water) and systemic vascular resistance (Rs; E-G; N=14 for CO2-enriched water and N=6 for acidified water) in tambaqui Colossoma macropomum. The shaded areas represent the 20 s period of injection. (D,H) The peak changes in fH (fH; D) and Rs (Rs; H) for injections of air-equilibrated water and water equilibrated with 1, 3, 5 or 10% CO2 in air. Values are means ± 1 S.E.M. An asterisk denotes a statistically significant difference from the initial pre-injection value (one-way RM-ANOVA; P<0.001 for all CO2 injections; P=0.016 for injection of acidified water on fH in C). For peak responses, groups that do not share a letter are significantly different from one another (one-way RM-ANOVA; P<0.001 for both).