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Journal of Experimental Biology 163,317-332 (1992)
Published by Company of Biologists 1992

THE RELATIONSHIP BETWEEN OXYGEN CONSUMPTION AND ION LOSS IN A FRESHWATER FISH

RICHARD J. GONZALEZ ¹ and D. G. MCDONALD ²

¹ Department of Biology, McMaster University 1280 Main Street West, Hamilton, Ontario, Canada L8S 4K1; Present address: Department of Organismal Biology and Anatomy, The University of Chicago, 1025 East 57th Street, Chicago, IL 60637, USA
² Department of Biology, McMaster University 1280 Main Street West, Hamilton, Ontario, Canada L8S 4K1

An increase in the functional surface area (FSA) of the gills of freshwater fish facilitates increased oxygen consumption (M_OO2) but also increases ion loss across the gills - a phenomenon that has been termed the osmorespiratory compromise. This study on the rainbow trout confirms that Na⁺ loss (J_out^Na) accelerates with increasing MO₂ but also shows that the former always exceeds the latter, i.e. the ion/gas ratio (IGR, J_out^Na/M_O2) increases. Since an increase in FSA should affect J^Na_out and M_O2 equally, the increase in the IGR is attributed to an increase in ion permeability and is thought to arise through opening of paracellular diffusion channels via disruption of tight junctions – a conclusion supported by the effects of brief osmotic shock, low external Ca²⁺ concentration and catecholamine infusion on ion losses across the gills. By analogy with extensive studies on ‘leaky’ epithelia, these treatments disrupt tight junctions by cell shrinkage, by displacement of Ca²⁺ from tight junction surfaces or by increasing intralamellar pressure, respectively. While enforced exercise or handling stress substantially increased the IGR of the trout above routine levels, animals were also capable of reducing IGR to about one-tenth of routine levels. This regulation may, in part, be due to decreasing intralamellar pressure, achieved in part by down-regulation of adrenergic receptors, but there appears to be a significant additional level of control that is probably exerted directly at the tight junctions. Such a degree of control is only possible, however, if animals do not continue to exercise and if Ca²⁺ levels in the water are not reduced. With continued exercise, the IGR returns to routine levels. Consequently, ion losses remain substantially elevated, suggesting that they may ultimately limit maximum sustainable activity. Measurement of the IGR under routine conditions is proposed as a simple means of predicting ion losses during activity and of analyzing the nature of the osmorespiratory compromise.

Key words: gas exchange, ion regulation, gill function, freshwater fish, osmorespiratory compromise, Oncorhynchus mykiss

Accepted on October 16, 1991

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