Cardiorespiratory adjustments during hypercarbia in rainbow trout Oncorhynchus mykiss are initiated by external CO(2) receptors on the first gill arch.

Abstract

Experiments were performed to test the hypothesis that the marked ventilatory and cardiovascular responses to hypercarbia in rainbow trout Oncorhynchus mykiss arise from specific stimulation of chemoreceptors localised to the first gill arch. This was accomplished by measuring cardiorespiratory variables during acute hypercarbia (20 min at P(CO(2))=8 mmHg; 1 mmHg=0.133 kPa) in fish subjected to selective bilateral extirpation of the first gill arch. The cardiovascular responses to hypercarbia in the intact fish included a significant bradycardia (from 75.0+/-1.6 to 69.0+/-2.0 beats min(-1); means +/- S.E.M.; N=16), an increase in dorsal aortic blood pressure (from 30.8+/-1.5 to 41.9+/-2.5 mmHg; N=16) and a rise in systemic vascular resistance (from 1.1+/-0.1 to 1.4+/-0.1 mmHg ml(-1) kg(-1) min(-1); N=16). Removal of the first gill arch or pre-treatment with the muscarinic receptor antagonist atropine prevented the hypercarbic bradycardia without affecting the pressure or resistance responses. Correlation analysis, however, revealed shallow but significant inverse relationships between water P(CO(2)) and cardiac frequency in both atropinised (r(2)=0.75) and gill-extirpated (r(2)=0.90) fish, suggesting a direct mild effect of CO(2) on cardiac function. The ventilatory response to hypercarbia in the intact fish consisted of an increase in ventilation amplitude (from 0.62+/-0.06 to 1.0+/-0.13 cm; N=16) with no change in breathing frequency. Removal of the first gill arch lowered resting breathing frequency and prevented the statistically significant elevation of breathing amplitude. Gill extirpation, however, did not totally abolish the positive correlation between water P(CO(2)) and ventilation amplitude (r(2)=0.84), suggesting the presence of additional (although less important) chemoreceptive sites that are not confined to the first gill arch. Plasma catecholamine levels were elevated during hypercarbia, and this response was unaffected by prior gill extirpation. To assess whether the CO(2) chemoreceptors of the first gill arch were sensing water and/or blood P(CO(2)), bolus injections of CO(2)-enriched water or saline were made into the buccal cavity or caudal vein, respectively. Injections of CO(2)-enriched water to preferentially stimulate external receptors evoked catecholamine release and cardiorespiratory responses that closely resembled the responses to hypercarbia. As in hypercarbia, extirpation of the first gill arch prevented the bradycardia and the increase in ventilation amplitude associated with externally injected CO(2)-enriched water. Except for a slight decrease in cardiac frequency (from 73.0+/-2.8 to 70.3+/-3.5 beats min(-1); N=11), injection of CO(2)-enriched saline to preferentially stimulate internal chemoreceptors did not affect any measured variable. Taken together, these data indicate that, in rainbow trout, the bradycardia and hyperventilation associated with hypercarbia are triggered largely by external CO(2) chemoreceptors confined to the first gill arch.