Consequences of catecholamine release on ventilation and blood oxygen transport during hypoxia and hypercapnia in an elasmobranch Squalus acanthias and a teleost Oncorhynchus mykiss
The marine dogfish (Squalus acanthias) and the seawater-adapted rainbow trout (Oncorhynchus mykiss) were exposed to acute environmental hypercapnia or hypoxia to evaluate (i) the dynamics of catecholamine release into the circulation and (ii) the impact of catecholamine release on gill ventilation and blood oxygen transport. This comparison was undertaken to test the hypothesis that the pattern and consequences of catecholamine release differ in the two species according to the presence or absence of a Root effect and a red blood cell (rbc) ss-adrenergic response. Hypercapnia and hypoxia elicited marked increases in plasma catecholamine levels in the trout but not in the dogfish. In the trout, catecholamine release occurred abruptly during hypoxia when arterial PO2 (PaO2) decreased below 2.7 kPa. In the dogfish, plasma catecholamine levels remained stable during hypoxia even when PaO2 fell below 2.0 kPa. Trout and dogfish displayed pronounced hyperventilatory responses during both hypercapnia and hypoxia. In trout, the hyperventilatory response consisted of an increase in ventilation amplitude (estimated by opercular cavity pressure changes) with no change in ventilation frequency (fv), whereas in the dogfish, both amplitude (estimated by spiracular cavity pressure changes) and fv increased significantly. The use of an extracorporeal circulation and frequent blood sampling demonstrated that plasma catecholamine levels and ventilation amplitude were not correlated during hypoxia in either species. During hypercapnia in trout, the bolus injection of a catecholamine cocktail (final nominal circulating levels 200 nmol l-1 adrenaline, 50 nmol l-1 noradrenaline) caused a rapid (within 2 min) 33 % reduction in ventilation amplitude that persisted for 3 min; fv was unaffected. This hypoventilatory response occurred concurrently with activation of rbc Na+/H+ exchange and an increase in arterial blood O2 content (CaO2) and O2 specifically bound to haemoglobin (O2/Hb). During hypoxia in trout, a similar injection of catecholamines activated rbc Na+/H+ exchange and increased O2/Hb yet was without effect on ventilation amplitude or fv. In dogfish during hypercapnia or hypoxia, injection of a catecholamine cocktail (final nominal circulating levels 125 nmol l-1 adrenaline, 125 nmol l-1 noradrenaline) caused slight but significant reductions in fv (3-4 min-1) without affecting ventilation amplitude. Catecholamine injections did not affect blood oxygen transport in dogfish. The results demonstrate significant differences in the nature of catecholamine release in dogfish and trout that may reflect, in part, the absence of a Root effect and rbc adrenergic Na+/H+ exchange in the elasmobranch. The present data do not support the hypothesis that circulating catecholamines play a major role in controlling breathing during hypoxia or hypercapnia.
Perry
S
Gilmour
K